SWEEP STAKE S REPR ODUCTIVE SUCCE SS IN HIG … · HEDGECOCK AND PUDOVKIN : SWEEPSTAKES REPRODUCTIVE SUCESS 973 leaves an average of two o spring for replacement; further, with SRS,

971

BULLETIN OF MARINE SCIENCE 87(4)971ndash1002 2011httpdxdoiorg105343bms20101051

Bulletin of Marine Sciencecopy 2011 Rosenstiel School of Marine and Atmospheric Science of the University of Miami

SweepStakeS RepRoductive SucceSS in HigHly Fecund MaRine FiSH and SHellFiSH

a Review and coMMentaRy

Dennis Hedgecock and Alexander I Pudovkin

abStRact

Most marine animal species are very abundant relatively long-lived and late-maturing with highly fecund adults adapted to spatially and temporally fluctuating ocean environments adults typically produce millions of small eggs that develop rapidly without parental care into planktonic larval stages that suffer high early mortality (type iii survivorship) yet large marine populations generally have only fractions of the genetic diversity expected from their sheer abundance and despite widely dispersing larvae and geographically weakly structured adult populations often show chaotic genetic heterogeneity on small spatial scales These paradoxical observations can be explained by the hypothesis of Sweepstakes Reproductive Success (SRS) which posits extremely large variance in individual reproductive success owing to sweepstakes-like chances of matching reproductive activity with oceanographic conditions conducive to gamete maturation fertilization larval development settlement and recruitment to the adult spawning population The primary genetic consequence of SRS is reduction of NeN the ratio of effective to actual population numbers to a value usually much smaller than 001 published nearly 30 yrs ago SRS has gained traction with numerous papers verifying specific predictions of the hypothesis in a broad array of marine animal taxa Moreover the hypothesis and empirical data from marine systems have stimulated modifications of coalescence population genetics theory which can now account for low molecular diversity and chaotic patchiness Here we review the empirical and theoretical support for SRS concluding that it plays a major role in shaping marine biodiversity comment on issues related to hypothesis testing and data interpretation and clarify some misconceptions

The idea that highly fecund marine animals might have smaller than expected effective population sizes because of high variance in individual reproductive success is nearly 30 yrs old (Hedgecock et al 1982) it was voiced independently as a potential explanation for a lack of variation in mtdna sequences given current population sizes (avise et al 1988 palumbi and wilson 1990 beckenbach 1994) and began to be known more widely after presentation at the genetics and evolution of aquatic organisms conference held in bangor wales September 10ndash16 1992 and subsequent publication of that conferencersquos proceedings (Hedgecock 1994a) Hedgecock (1994a) coined the term ldquoSweepstakes Reproductive Successrdquo (SRS) to describe the chances of a highly fecund marine animal contributing offspring to a future pool of reproductively mature adults a process envisioned to have relatively few ldquowinnersrdquo and many ldquolosersrdquo only in the last decade or so has SRS been cited more frequently than in preceding decades as a potential explanation for patterns of genetic diversity in marine populations (eg Moberg and burton 2000 Hauser et al 2002) been tested explicitly (eg li and Hedgecock 1998 turner et al 1999 2002 Flowers et al 2002) or explored theoretically (eg eldon and wakeley 2006 Sargsyan and wakeley 2008 eldon and wakeley 2009 eldon 2009) Here we restate

OA Open access content

972 BULLETIN OF MARINE SCIENCE VOL 87 NO 4 2011

the hypothesis discuss its predictions and the methods for and limits to testing those predictions review evidence that has accumulated for the hypothesis and finally draw implications about the place of SRS in contemporary marine science

the Hypothesis of Sweepstakes Reproductive Success

Most marine animals have ecologically distinct adult and larval stages with high fecundity and high early mortality or type iii survivorship (Thorson 1950 winemiller and Rose 1992) larvae of such species typically develop for weeks in the plankton are microscopic weakly swimming easily dispersed by ocean currents and subject to high mortality resulting in erratic recruitment to adult populations (cushing 1990) Survival growth and behavior of these larval forms influence recruitment success population connectivity and the distribution and abundance of adult populations (cowen et al 2006 2007) which tend to occupy vast geographic ranges and often comprise tens of millions to billions of individuals in many cases based on catch statistics yet these large marine populations generally have only fractions of the genetic diversity expected from their sheer abundance (Hedgecock et al 1982 nei and graur 1984 avise et al 1988 palumbi and wilson 1990 avise 1994 grant and bowen 1998) and despite widely dispersing planktonic larvae and high genetic similarity over broad spatial scales often show chaotic genetic heterogeneity on small spatial scales (Johnson and black 1984 watts et al 1990 Hedgecock 1994b edmands et al 1996 david et al 1997 recent literature reviewed by Hauser and carvalho 2008) to explain both of these paradoxical observations one of us (dH) hypothesized that marine animals in general have extremely large variance in individual reproductive success owing to sweepstakes-like chances of matching reproductive activity with oceanographic conditions conducive to gamete maturation fertilization larval development settlement and recruitment to the adult spawning population (Hedgecock et al 1982 p 322ndash324 Hedgecock 1982 Hedgecock 1994a)

the population genetic effect of SRS is captured by wrightrsquos (1938) equation Ne asymp (4N minus 2) ∕(Vk + 2) in which Ne is the effective population size N is the size of the breeding population and Vk is the variance in number of offspring (k) con-tributed per parent to the adult spawning population in the Fisher-wright model of a diploid population with non-overlapping generations and constant size kr = 2 Vk asymp 2 (ie the variance of a poisson or binomial distribution of offspring number) and Ne asymp N in real populations Vk may exceed that of the ideal population reducing Ne relative to N (see crow and denniston 1988) The SRS hypothesis says that Vk is often large enough in highly fecund marine animal populationsmdash102 and potentially much highermdashto reduce the ratio of effective to actual population numbers NeN asymp 4 (Vk + 2) to a small fraction (ltlt 001) Though somewhat arbitrary this quantitative defini-tion of SRS contrasts sharply both with the theoretical conclusion that the NeN ratio should rarely be below 05 (nunney 1996) and also with a meta-analysis reporting an average NeN ratio of 011 across 192 studies mostly of terrestrial species taking fluctuating population size unequal sex ratio and variance in reproductive success into account (Frankham 1995) Though Vk is certainly enhanced in marine species by widespread failure to reproduce Hedrick (2005) shows that a few very successful breeders can make the NeN ratio small even if a sizeable fraction of the population

hEdgECOCk ANd pUdOVkIN SwEEpSTAkES REpROdUCTIVE SUCESS 973

leaves an average of two offspring for replacement further with SRS the NeN ratio is close to NbN the ratio of the effective number of breeders Nb to the adult census size

although some have likened SRS to a bottleneck the two processes are conceptu-ally distinct and should not be confused a bottleneck is a one-time drastic reduc-tion in the adult population usually as a result of some catastrophic circumstance a bottleneck perturbs a population away from mutation-drift equilibrium and can have long-lasting effects on genetic diversity while the population recovers (nei et al 1974 tajima 1989b luikart and cornuet 1999) SRS on the other hand is a pro-cess largely uncoupled from spawning biomassmdashechoing the classic decoupling of stock biomass and recruitment success in fisheriesmdashand can take place without any change in census population size SRS thus produces a dynamic mutation-drift equilibrium that is driven by the environmental vagaries of reproductive success and that maintains much less genetic diversity than expected on the basis of large census size

variance in reproductive success is often synonymous with sexual selection in ter-restrial animals (clutton-brock 1988 see Rowe et al 2008 for evidence of sexual selection in experimental populations of atlantic cod) but the causes of SRS are primarily envisioned as stochastic fluctuations in the ocean environment (cushing 1990 waples 1998) The SRS hypothesis indeed follows from the matchmismatch explanation for variance in recruitment to fisheries (Hjort 1914 cushing 1990) but extends that idea to the level of individual rather than stock reproductive success and expands the focus from larval survival alone to all phases of reproduction includ-ing maturation spawning fertilization larval growth and survival metamorphosis settlement and recruitment to the adult population a major implication of SRS is that random genetic drift may be occurring on the same time-scale as marine re-cruitment dynamics Thus SRS and population-genetic approaches to testing it are highly relevant to research on marine population connectivity (cowen et al 2007 Hedgecock et al 2007a)

it should come as no surprise then that just as recruitment success in marine fish-eries fluctuates greatly so too may severity of SRS fluctuate a species that may show evidence for SRS in one place (Hedgecock et al 2007b) may not show evidence for it at another time or in another place (taris et al 2009 see ldquolimitations in testing SRS predictionsrdquo) The relevant time-scales issues of overlapping generations and statis-tical power for testing SRS predictions need to be considered carefully in empirical studies of the hypothesis

The role of high fecundity in the SRS hypothesis requires clarification a miscon-ception that under SRS high fecundity causes high Vk and low NeN ratios is clari-fied later Here we wish to point out that while marine fish and invertebrates with female fecundities of many millions of eggs certainly have the potential for sweep-stakes reproduction and high Vk SRS may also occur in species having more modest fecundities The fecundity necessary for SRS to occur need only be on the same scale as local or regional recruitment in the case of the white seabream Diplodus sargus (linnaeus 1975) for example fecundity on the order of tens of thousands can ac-count for temporal variation among recruiting cohorts numbering in the hundreds (lenfant and planes 2002) if successful reproduction by a few individuals can re-place the local or regional population sampled then SRS is possible


predictions of the SRS HypothesismdashThe SRS hypothesis predicts first that random genetic drift which is inversely proportional to Ne may be observable in adult populations sampled over sufficient intervals of time This prediction can be tested by sampling the adult population over generations and looking for statistically significant shifts in allelic frequencies that cannot be explained by mutation selec-tion migration or varying year-class strengths in populations with overlapping gen-erations (krimbas and tsakas 1971 nei and tajima 1981 pollak 1983 waples 1989 Jorde and Ryman 1995 2007) The effect of overlapping generations can be handled with life-table data (Jorde and Ryman 1995 1996 2007) usually the time-scale of temporal studies is short enough to ensure that mutation is not a factor Selection on genetic markers is assumed to be weak or non-existent and can be evaluated in any case by comparing observations to the statistical distribution of temporal variance across markers under the null hypothesis of no selection (lewontin and krakauer 1975 nei and tajima 1981 Hedgecock and Sly 1990) Migration is more difficult to dismiss as a potential explanation (cf wang and whitlock 2003) unless there is independent evidence that the study population is isolated (li and Hedgecock 1998 liu and ely 2009) nevertheless migration becomes an untenable explanation for temporal variation when allele-frequency variance among adult populationsmdashas measured for example by wrightrsquos (1931) FST statistic which is lt 0001 in most ma-rine animal species (Hauser and carvalho 2008)mdashis less than allele-frequency vari-ance among recruits (watts et al 1990 Moberg and burton 2000)

The hypothesis also makes predictions about levels of genetic diversity within and among progeny cohorts produced by sweepstakes reproductive events (Hedgecock 1994a) For example under SRS a cohort of progeny produced by a single episode of spawning should have less allelic diversity and possibly higher linkage disequilib-rium than the adult population in severe cases relatedness might be higher within a cohort than between a cohort and the adult population or other cohorts Moreover under SRS allele-frequency variance among cohorts should be larger than allele-frequency variance among adult populations

Finally the SRS hypothesis is amenable to testing by the comparative method For example low fecundity marine species with type ii survivorship such as sharks and marine mammals should not be capable of large Vk and should show high NeN ra-tios such as the value of 045 reported for the sandbar shark (portnoy et al 2009 see also their fig 1 and references regarding high NeN ratios in marine mammals) com-parison of closely related species having contrasting modes of larval developmental (planktotrophic or lecithotrophic larvae or crawl-away juveniles hatched from ben-thic egg capsules) has nearly a 40-yr history in marine population genetics (berger 1973) This literature shows in general though with numerous exceptions that FST is inversely correlated with dispersal potential (gyllensten 1985 waples 1987 palumbi 1994 ward et al 1994 bohonak 1999 Hellberg 2009) Recently lee and boulding (2009) using four species of the marine gastropod Littorina expanded on this com-parative approach by affirming an SRS prediction that low-dispersal low-fecundity species should show spatial subdivision but temporal stability while high-dispersal high-fecundity species should show low or no spatial variation but should vary tem-porally owing to SRS

The foregoing predictions are about contemporary populations and demographic processes However SRS also predicts that marine animal populations maintain less molecular genetic diversity over evolutionary time-scales than expected from their


abundance as we shall review these predictions are elegantly articulated by coales-cence models that accommodate the simultaneous multiple mergers (multifurcat-ing genealogies) implied by the SRS hypothesis (eldon and wakeley 2006 wakeley and Sargsyan 2009) SRS predicts shallow genealogies in marine animal popula-tions ldquostarrdquo phylogenies of dna sequences and haplotype networks in which inte-rior nodes are represented by extant individuals and average nucleotide differences among sequences are much less than expected given the number of segregating sites (beckenbach 1994 grant and bowen 1998 Sargsyan and wakeley 2008)

limitations in testing SRS predictionsmdashwhile SRS makes testable predic-tions any one test may be limited by uncontrolled conditions or by low power to reject the null hypothesis of low Vk and high NeN ratio (ie gtgt 001) when SRS is true one limitation in testing the hypothesis has already been mentioned the role of variability in the underlying environmental causes of SRS a study can be done in the right place but at the wrong time For example in a population of the pacific oyster Crassostrea gigas (Thunberg 1793) in dabob bay washington which has a census size in the tens of millions the rate of random genetic drift and the estimate of Ne calculated from the reciprocal of this rate using the temporal method (see below) vary temporally between 1985 and 1990 genetic drift was weak giving rise to an estimate of Ne asymp 500 with an infinite upper confidence limit between the early 1970s and 1990 however genetic drift was stronger yielding an estimate of Ne asymp 200ndash400 with a finite upper confidence limit (Hedgecock 1994a) likewise between 1990 and 1994 a period that included years of poor recruitment genetic drift was again quite strong yielding Ne asymp 50 also with a finite upper confidence limit (d Hedgecock unpubl data) The rate of genetic drift varies because variability in ocean conditions affects variance in individual reproductive success drift in the oyster population would not have been detected had the study been done only with the 1985 and 1990 samples

a limitation to testing SRS with cohort studies is the difficulty of defining and sampling true cohorts of progeny spawned at the same time in the same region to the extent that a ldquocohortrdquo sample incorporates individuals from different bouts of reproduction the SRS signal is diluted in practice cohorts are sampled at varying times after spawning up to settlement or even later if identified from size-frequency distributions or in the case of some fishes or invertebrates from growth rings in otoliths or shell parts Recruits in some studies for example are defined by cutoffs in the size-frequency distributions of post-metamorphic juveniles and adults (tracey et al 1975 Johnson and black 1982 1984 watts et al 1990 edmands et al 1996 Moberg and burton 2000) a practice which undoubtedly groups individuals spawned at very different times (despite this limitation cohort studies have revealed evidence in support of SRS) cohort studies can be further improved by collecting samples appropriate to testing the hypothesis to the extent that recruits can be sorted into year classes and settlement has a major annual peak year classes may more closely represent true reproductive cohorts (Johnson and black 1982 1984 calderoacuten et al 2009) likewise collections of fish larvae from standard monitoring units for the recruitment of reef fishes (ammann 2004) sampled at intervals of days or weeks yield recruits that are likely to have been spawned at the same time (Selkoe et al 2006)

predictions of the SRS hypothesis are often tested by estimation of Ne or Nb and the census population size N Fortunately methods for estimating effective


population or effective breeding numbers have expanded and improved recently thanks to the advent of dna markers and high-throughput genotyping methods and advances in statistical analysis (luikart et al 2010) Statistical and sampling design issues encountered in estimating N Ne or Nb from demographic or genetic data are discussed in depth elsewhere (waples 1998 berthier et al 2002 palstra and Ruzzante 2008 luikart et al 2010 pudovkin et al 2010) Statistical power may often be limiting in tests of SRS not only in the technical sense relating to the numbers of markers and individuals genotyped but also in the methodological sense of not being able to distinguish very small from moderate effective population sizes The recruitment sweepstakes can have many winners (cf Flowers et al 2002) because 103ndash105 winners might still constitute only a small proportion (ltlt 001) of the adult population present methods rarely permit finitely bounded estimates of Ne greater than hundreds or a few thousand (luikart et al 2010) while a small population will rarely be mistaken for a large one the size of a moderately large population is difficult to estimate with present technology (waples and do 2010) This limitation makes the many observations of finite Ne in abundant marine fishes and invertebrates all the more remarkable (Hauser and carvalho 2008)

There are limitations in estimating historical Ne from molecular data First cur-rent methods for estimating long-term Ne rely on the standard kingman coales-cent which is restricted to bifurcating genealogies and is thus not appropriate for modeling the multifurcating genealogies implied by SRS (eldon and wakeley 2006 Sargsyan and wakeley 2008) However sample sizes larger than the number of suc-cessful parents may be required to distinguish a multiple-merger coalescent from the standard kingmanrsquos coalescent (wakeley and Sargsyan 2009) Second long-term estimates of N are also needed to interpret the evolutionary NeN ratio (Frankham 1995 nunney 1996 waples 2005) but are rarely available (cf grant and bowen 1998) Historical fluctuations in recorded catches of atlantic cod however were not large enough to reduce NeN to what was estimated from genetic methods 10minus5ndash10minus6 (Aacuternason 2004) Finally selective sweeps or population bottlenecks could also be responsible for low variation in mtdna especially since the whole mitochondrial genome is inherited as a unit such events also produce multiple-merger coalescents (Schweinsberg and durrett 2005 Sargsyan and wakeley 2008) and are therefore al-ternative explanations for star phylogenies

citation analyses

our review of SRS literature is based on 716 records extracted from the Thomson Reuters iSi web of ScienceSM (woS httpwokinfocomproducts_toolsmultidis-ciplinarywebofscience) These records consist of nine core papers in the history of the SRS hypothesis (Hedgecock 1982 Hedgecock et al 1982 Hedgecock and Sly 1990 Hedgecock et al 1992 Hedgecock 1994ab li and Hedgecock 1998 Hedgecock et al 2007ab) and all the papers citing them (as of May 13 2010) we also include in this bibliography the paper by beckenbach (1994) which independently put forward the hypothesis of high variance in reproductive success and the 18 papers citing it The bibliography is available as a comma delimited file in supplemental online ma-terial (SoM table 1) and at httpgarfieldlibraryupenneduhistcomphedgecock

to handle and explore this sizable bibliographic database we used Histcite soft-ware (httpwwwhistcitecom) which allows correction of inaccuracies in woS ci-


tation numbers owing to authorsrsquo mistakes and quick sorting of records by date author journal title words and frequencies of citation either globally in the woS (gcS) or locally in the database (lcS) making bibliographic information visible and easy to manage These Histcite functions are available for the online version of the database cited above a unique feature of Histcite software is the cumulative list of cited references extracted from all records of the bibliography in our case this cited Reference list comprises 23527 works the list gives the number of records in the database citing each work This feature allows one to check for thematically related papers which may not have been cited by one of the core references used to form the bibliography but which may have been frequently cited by others working in the field we do not identify any other papers about SRS in the cited Reference list suggesting that our database of SRS literature is complete Many of the most-shared cited refer-ences are reviews (eg Frankham 1995) methods papers (eg waples 1989) or early papers in marine population genetics (Johnson and black 1984) many of which are cited here as well Histcite software and the procedures of compiling bibliographies to be processed by it are discussed by garfield et al (2002 2003)

This bibliography is used first to illustrate yearly growth in interest in the SRS hy-pothesis (Fig 1) For this purpose we extract counts by year of 602 papers that cite at least one of six key SRS papers (Hedgecock 1982 Hedgecock et al 1982 Hedgecock and Sly 1990 Hedgecock et al 1992 Hedgecock 1994ab) growth in SRS literature became more pronounced after 1997 possibly as publications such as Ruzzante et al (1996 lcS 57) li and Hedgecock (1998 lcS 93) waples (1998 lcS 76) Hauser et al (2002 lcS 46) turner et al (2002 lcS 45) and Flowers et al (2002 lcS 43) brought the hypothesis to the attention of a wider audience

Histcite also generates ldquohistoriographsrdquo showing citation links between papers For example we illustrate the milieu of SRS literature using the top 33 papers

Figure 1 Frequency histogram by year (through 2009 decades denoted by pattern) of publica-tions citing key papers published between 1982 and 1994 on the hypothesis of Sweepstakes Reproductive Success in marine animal populations (see text for description of citation database)


obtained by sorting the full bibliography of 716 papers for lcS to these 33 papers we add again the historically important paper by beckenbach (1994) The resulting historiograph (Fig 2a) distinguishes on the far right a subset of papers related more to the issues of gene flow and population or stock structure (Fig 2 nodes 2 5 26 99 138 174 213 and 316) than to the development and testing of SRS per se these papers and topics are not discussed in our review also excluded from our review are papers about reproductive success in hatchery stocks (such as nodes 68 and 324 which do not have subsequent citations by papers in this subset) The independence of beckenbachrsquos (1994) paper (node 89 Fig 2) is illustrated by the lack of connections to earlier papers in the network that it is subsequently cited by only two of the top SRS papers suggests that this seminal paper was overlooked by subsequent workers possibly because it was published in a specialized book about molecular evolution important papers in the early growth of SRS literature are the three highly cited nodes in the center of the network (Ruzzante et al 1996 node 137 li and Hedgecock 1998 node 180 waples 1998 node 198) These are followed most immediately by

Figure 2 Historiograph of the top 33 papers in the HistCite bibliography sorted by Local Citation Score (LCS the number of papers in the collection siting each paper) plus Beckenbach (1994) Each node represents a paper lines with arrows show citation links The 34 nodes have 132 links Size of each node is proportional to LCS shaded nodes are 10 core papers used to produce the bibliography Nodes are 1 Hedgecock et al (1982) 2 Hedgecock (1982) 5 Burton (1983) 26 Hedgecock (1986) 50 Hedgecock and Sly (1990) 63 Benzie et al (1992) 68 Gaffney et al (1992) 70 Hedgecock et al (1992) 88 Hedgecock (1994a) 89 Beckenbach (1994) 99 Hedgecock (1994b) 111 Frankham (1995) 127 Jorde and Ryman (1996) 137 Ruzzante et al (1996) 138 Bentzen et al (1996) 174 Shaklee and Bentzen (1998) 180 Li and Hedgecock (1998) 196 Grant and Bowen (1998) 198 Waples (1998) 213 Bohonak (1999) 262 Moberg and Burton (2000) 301 Launey and Hedgecock (2001) 316 Hellberg et al (2002) 324 Boudry et al (2002) 334 Flowers et al (2002) 339 Planes and Lenfant (2002) 341 Hauser et al (2002) 348 Turner et al (2002) 360 Taylor and Hellberg (2003) 440 Hoarau et al (2005) 446 Hedrick (2005) 469 Pujolar et al (2006) 535 Hedgecock et al (2007b) 557 Hedgecock et al (2007a)


five empirical studies with high local citation scores Moberg and burton (2000 node 262) and four papers in 2002 (left to right in Fig 2a) turner et al (2002 node 348) Hauser et al (2002 node 341) Flowers et al (2002 node 334) and planes and lenfant (2002 node 339)

an interesting alternative view of SRS literature is given by the historiograph in Figure 3 which was constructed by focusing on six theoretical papers by wakeley and colleagues (Fig 3 nodes 365 484 580 599 627 and 631) and all papers cited by or citing them with 26 nodes and only 79 links this network is not as intercon-nected as the network of empirical papers (Fig 2a) with its 34 nodes and 132 links These theoretical papers nevertheless clearly identify the origins of the SRS hypoth-esis (nodes in 1994 or earlier) including beckenbach (1994) and the chief empirical papers supporting it Surprisingly these theoretical papers are cited by several other theorists but by only one of nearly 100 empirical papers in the database for 2009 and 2010 (paacutelsson et al 2009 node 641) This suggests a current gap between theory and practice in marine population genetics to which we shall return

Figure 3 Historiograph of studies cited by and citing (shaded boxes) six theoretical papers by Wakeley and colleagues (bold boxes) size of boxes is not proportional to numbers of citations There are 26 nodes with 79 links in this network Nodes are 1 Hedgecock et al (1982) 5 Burton (1983) 88 Hedgecock (1994a) 89 Beckenbach (1994) 95 Boom et al (1994) 99 Hedgecock (1994b) 251 Aacuternason et al (2000) 320 Bekkevold et al (2002) 334 Flowers et al (2002) 348 Turner et al (2002) 365 Wakeley and Takahashi (2003) 402 Aacuternason (2004) 446 Hedrick (2005) 463 Saavedra and Pentildea (2005) 484 Eldon and Wakeley (2006) 511 Mohle (2006) 515 Murray and Hare (2006) 580 Eldon and Wakeley (2008) 599 Sargsyan and Wakeley (2008) 627 Wakeley and Sargsyan (2009) 631 Eldon and Wakeley (2009) 641 Paacutelsson et al (2009) 658 Taylor (2009) 670 Eldon (2009) 695 Berestycki et al (2010) 713 Luikart et al (2010)


temporal Studies

The SRS prediction of random genetic drift in adult marine animal populations was the first to be tested (Hedgecock and Sly 1990) and remains the most widely-tested SRS prediction owing in large part to earlier development of the temporal variance estimator of Ne (nei and tajima 1981 pollak 1983 waples 1989 luikart et al 2010) in their review of marine fisheries genetics Hauser and carvalho (2008 table 1) cited 15 studies of effective population size for marine species mostly fishes as diverse as the atlantic cod and european pilchard but also two invertebrates a crustacean the tiger prawn Penaeus esculentus Haswell 1879 (ovenden et al 2007) and a bivalve mollusc the european flat oyster Ostrea edulis linnaeus 1758 (Hedgecock et al 2007b) twelve of these 15 studies employed one or more statistical approaches to estimating Ne from temporal genetic data (see luikart et al 2010 for a review of methods) all 12 studies reported finite upper bounds on estimated Ne for at least one locality and NeN ratios averaging ~10minus4 altogether these studies provided taxonomically and geographically broad support for the SRS hypothesis even if there were bias against publishing negative results to the studies reviewed by Hauser and carvalho (2008) should be added the formative study of temporal change in hatchery and wild populations of the pacific oyster (Hedgecock and Sly 1990) developed further by Hedgecock (1994a) for the population of pacific oysters in dabob bay washington and an early look at genetic drift in hatchery-propagated aquaculture stocks which included estimates for some wild oyster populations (Hedgecock et al 1992)

Several early studies of temporal genetic variation were not included in Hauser and carvalho (2008 table 1) presumably because they assessed the significance of allele-frequency change but did not estimate Ne or the NeN ratio These include studies that found significant temporal genetic variance in atlantic cod Gadus morhua linnaeus 1758 (Ruzzante et al 1996) surf clam Spisula ovalis (J Sowerby 1817) (david et al 1997) european hake Merluccius merluccius linnaeus 1758 (lundy et al 2000) walleye pollack Theragra chalcogramma (pallas 1814) (olsen et al 2002) penaeid shrimp (ball and chapman 2003 barcia et al 2005) and european eel Anguilla anguilla linnaeus 1758 (dannewitz et al 2005 Maes et al 2006) in several of these studies neither SRS nor alternative explanations for temporal variation (eg immigration or transient use of spawning grounds by genetically differentiated subpopulations) could be definitively falsified leaving SRS as one of several possible explanations Several early studies of freshwater fish and the amphidromous ayu Plecoglossus altivelis (temminck and Schlegel 1846) which have fecundities approaching those of marine fishes also provided support for the SRS hypothesis (alo and turner 2005 turner et al 2006 yamamoto et al 2007)

Thirty-eight studies in our citation database which were published after mid-2007 (therefore mostly after the Hauser and carvalho review) had ldquotemporalrdquo ldquotemporal-lyrdquo or ldquotimerdquo in the abstract suggesting growing interest in the temporal dimension of marine population genetic variation Five studies used the temporal method to es-timate Ne with four reporting finite upper bounds on at least some estimates (borrell et al 2007 lee and boulding 2007 chevolot et al 2008 larsson et al 2010) and one reporting a finite estimate of Ne but with an infinite upper bound (Han et al 2008) liu and ely (2009) estimated that a population of 362000 striped bass in a freshwater river system had Ne = 93 and thus NeN asymp 26 times 10minus4 From temporal genetic change


in isolated experimental populations of perch Perca fluviatilis linnaeus 1758 and roach Rutilus rutilus (linnaeus 1758) demandt (2010) estimated finite Ne and NeN ratios of 10minus2ndash10minus3 suggesting again that certain freshwater fish have sufficient fe-cundity and the necessary environmental conditions for SRS to work

other recent studies of marine or estuarine species report significant temporal variance in allele frequencies without estimating Ne (papetti et al 2009 lee and boulding 2009 Hepburn et al 2009 pumitinsee et al 2009 varela et al 2009 Han et al 2010 Marino et al 2010 ng et al 2010) Four studies that examined genetic variation among age classesmdashby counting otolith annuli in white seabream D sar-gus (gonzaacutelez-wanguumlemert et al 2007) and european eels (palm et al 2009) and seasonal growth rings in the arctic surfclam Mactromeris polynyma (Stimpson 1860) (cassista and Hart 2007) and the common sea urchin Paracentrotus lividus (lamarck 1816) (calderoacuten et al 2009)mdashreport little or no temporal change year-classes as noted above can comprise multiple cohorts of recruits which would bias against detection of SRS and may explain why studies in which age classes are taken as temporal samples have failed to find evidence of temporal variance

cohort Studies

Marine population geneticists were subsampling size-classes to compare ldquorecruitsrdquo to sub-adults or adults nearly a decade before SRS became widely known (tracey et al 1975 Milkman and koehn 1977 koehn et al 1980 Johnson and black 1982 1984 gosling and wilkins 1985 watts et al 1990 kordos and burton 1993 edmands et al 1996) Johnson and black (1982 1984) concluded that ldquochaotic patchinessrdquo in the genetic composition of benthic adult populations was caused by temporal patchi-ness in the genetic composition of recruits and could not be explained by delivery of larvae from different source populations or by post-settlement selection they at-tributed such patchiness instead to selection on larvae in the plankton in one of the first studies to compare the genetics of larvae and adults kordos and burton (1993) showed greater levels of spatial and temporal variation among samples of megalopae of the blue crab Callinectes sapidus M J Rathbun 1896 than among samples of adults considering SRS unlikely kordos and burton instead attributed their obser-vation to temporal variation in the provenance of megalopae delivered to the texas coast in several subsequent studies varying provenance of larvae was ruled out as an explanation of greater variation among recruits than adults by the relative ho-mogeneity of adult populations (edmands et al 1996 Johnson and wernham 1999 Moberg and burton 2000 burford and larson 2007 christie et al 2010)

development of highly polymorphic dna markers and statistical methods for determining genetic properties of cohorts produced by small numbers of parents (ie diversity among cohorts linkage disequilibrium excess heterozygosity relatedness) has more recently enabled diverse and specific tests of SRS predictions in many of these cases the effective number of parents of a cohort Nb can be determined using ldquoone-samplerdquo estimators based on excess heterozygosity (pudovkin et al 1996 2010) or linkage disequilibrium (Hill 1981 waples 2006 waples and do 2008 2010 see review of luikart et al 2010) use of multiple methods of cohort genetic analysis can often detect signals of SRS whether Nb can be estimated with confidence (Hedgecock et al 2007b) or not (christie et al 2010)


diversity and RarefactionmdashThe simplest SRS prediction about cohortsmdashthat they should have less diversity than samples from the adult populationmdashis one of the least tested Results from some early allozyme studies comparing adults and recruits were consistent with this SRS prediction genetic diversity in such comparisons is best measured by haplotype or allelic richness adjusted for sample size (leberg 2002 kalinowski 2004) since observed heterozygosity can actually be inflated by allele-frequency differences between males and females (pudovkin et al 1996) or by greater evenness of allelic frequencies following loss of alleles (Hedgecock and Sly 1990) Hedgecock et al (2007b) compared diversity of juvenile and adult samples of the european flat oyster using a rarefaction estimate of Nb in this method the significance of the difference in allelic diversity between adults and progeny was assessed through simulations of cohorts made by drawing finite numbers of parents from an adult population with the same allelic diversity as the one observed This method yielded an estimate of Nb asymp 14 with a 95 confidence interval of 10ndash18 which was concordant with estimates produced by three other methods (Hedgecock et al 2007b)

a second predictionmdashthat there should be more diversity among cohorts than among samples from the adult populationmdashhas been upheld in several studies in the first large study of larvae using microsatellite dna markers Ruzzante et al (1996) found heterogeneity among larval cod samples that they attributed to SRS and not to different source populations li and Hedgecock (1998) provided a direct test of the SRS cohort prediction by demonstrating changing frequencies of mtd-na polymorphisms among pacific oyster larvae collected during a single spawning season in dabob bay a population with significant genetic drift and very low NeN ratio (Hedgecock 1994a) Studies of recruiting white seabream D sargus in the bay of banyuls also reported significant genetic differences among cohorts (lenfant and planes 2002 planes and lenfant 2002) More recent studies (eg burford and larson 2007 liu and ely 2009 christie et al 2010) have continued to find evidence for re-duced variation within cohorts and enhanced variation among cohorts compared to variation among adult populations

osborne et al (2005) found genetic differences among pelagic egg samples and be-tween egg and adult samples of the federally endangered Rio grande silvery minnow Hybognathus amarus (girard 1856) which they interpreted as resulting from high variance in reproductive success diversity among cohorts of larval sutchi catfish Pangasius hypophthalmus (Sauvage 1878) provided further support for applicability of the SRS hypothesis to some freshwater fishes (So et al 2006)

Flowers et al (2002) rejected ldquoextreme sweepstake eventsrdquo for the purple sea urchin calling into question ldquothe general significance of this (SRS) phenomenonrdquo However this study was a weak test of SRS because it compared mtdna sequence polymorphisms from 283 newly settled recruits to 145 sequences previously obtained by edmands et al (1996) 43 of which were from recruits not adults (S edmands university of Southern california pers comm) as discussed above low power to reject moderate SRS in this study and others of its type remains a limitation in testing SRS and quantifying its consequences

Heterozygote excessmdashwhen the number of parents is very small there will be an excess of heterozygotes observed in the progeny Ho with respect to the number of heterozygotes expected under random mating He such that the effective number


of breeders Nb may be estimated as a simple function of the standardized deviation from random-mating proportions of heterozygotes D = (Ho minus He)He (pudovkin et al 1996) The statistical properties of this ldquoheterozygote-excessrdquo or ldquoDrdquo estimator have been well explored (luikart and cornuet 1999 pudovkin et al 2010) for Nb le 30 sample sizes of 200 or more progeny and 80 or more independent alleles yield an ac-curate estimate while for Nb of 50ndash100 a sample of 500ndash1000 progeny and 450ndash900 independent alleles are required despite these limitations Hedgecock et al (2007b) estimated from heterozygote excesses at three microsatellite dna markers Nb asymp 20 with a 95 confidence interval of 10ndash368 for a naturally produced cohort of juvenile flat oysters

linkage or gametic phase disequilibriummdashassociations in the frequencies of alleles at different though not necessarily linked gene loci are generated in popu-lations of finite size which is the basis of an estimator of Ne based on gametic phase or linkage disequilibrium (ld Hill 1981 waples 2005 2006) The great advantages of the ld-estimator are that it requires only a single sample and the amount of data used scales with the square of the number of loci and alleles assayed (waples and do 2010) For a cohort the ld-estimator should yield a number close to the effective number of parents Nb although recent bottlenecks can bias the estimate downwards (waples 2005) whether or not Nb is estimable from ld one might expect higher levels of ld in recruits than in adults under SRS owing to the finite number of par-ents contributing to cohorts Higher levels of ld in recruits compared to adults have been detected in several cohort studies (planes and lenfant 2002 Selkoe et al 2006 liu and ely 2009 christie et al 2010) which is consistent with SRS despite the ad-vantages of the ld method our database contains only two studies that used ld to estimate Nb (Hedgecock et al 2007b portnoy et al 2009) Hedgecock et al (2007b) found Nb asymp 275 (95 ci of 241ndash311) in a cohort of european flat oysters which is larger than the upper confidence limits of the temporal and rarefaction estimates of Nb for the same cohort but is within the confidence interval of the heterozygote-excess estimate

Relatednessmdashextreme cases of SRS could result in full- or half-siblings being included in a cohort sample Highly polymorphic microsatellite dna markers en-able the statistical testing of this SRS prediction Most studies have used software for computing the Queller-goodnight pairwise relatedness statistic and for testing pairwise relatedness against a simulated null-hypothesis of allele-sharing in a popu-lation having the same allele-frequency profile but no relatedness (goodnight and Queller 1999) with SRS however average relatedness among members of a cohort may not be significantly greater than zero even if the cohort contains some full- or half-siblings because the vast majority of pairs are likely to be unrelated (Selkoe et al 2006 buston et al 2009) various solutions to this problem have been offered (Hedgecock et al 2007b buston et al 2009) for example one can compare observed and expected proportions of full- or half-sibling pairs at various levels of signifi-cance (Herbinger et al 1997) using this approach Hedgecock et al (2007b) demon-strated more pairs at higher levels of significance than expected by chance

planes and lenfant (2002) and planes et al (2002) found significant average re-latedness within cohorts which they interpreted as signals of SRS a study of the acorn barnacle Semibalanus balanoides (linnaeus 1767) found remarkable related-ness among new recruits with eight of 37 samples showing average relatedness con-


sistent with full- or half-siblings (veliz et al 2006) although this barnacle has low fecundity (5000 larvae per female) hermaphroditism and extended sibships which were detected in this study by construction and analysis of sibship-networks were hypothesized to increase the scope of variance in reproductive success Selkoe et al (2006) were the first to present evidence for full- and half-sibs in recruits of a marine fish (five of 20 cohorts sampled) despite setting conservative thresholds for the sig-nificance of the relatedness statistic The more stringent the threshold for rejecting the null hypothesis of no relatedness the higher the likelihood is that true sibling pairs are missed (type ii error) pujolar et al (2009) similarly calculated genetic re-latedness among A anguilla glass eels and found that arrival waves were composed of ca 1ndash3 highly related individuals (half-sibs or full-sibs) plus a majority of un-related individuals together with previous evidence for temporal genetic patchi-ness and relatedness of individuals within cohorts (pujolar et al 2006) the weight of evidence for european eel suggests that they are subject to SRS The lesson to date from studies of within-cohort relatedness is that a small number of true siblings in a cohort may be difficult to detect and to quantify using pairwise measures of related-ness

liu and ely (2009) used sibship reconstruction (wang 2009) to show that striped bass have small Ne demonstrating the advantages of partitioning a cohort into sib-groups rather than relying on pairwise measures of relatedness unlike other meth-ods to test SRS partitioning a cohort into sibships (Smith et al 2001 wang 2004 2009) combined perhaps with reconstruction of parent genotypes (eg bucklin et al 2009) affords direct evidence for variance of reproductive success

Studies of coalescence

avise et al (1988) palumbi and wilson (1990) and beckenbach (1994) indepen-dently arrived at the hypothesis of SRS as a selectively neutral explanation of the high-ly skewed l-shaped frequency-profiles and ldquostarrdquo phylogenies of mtdna sequences in marine animal populations This pattern of mtdna diversity is now recognized to be common in marine animal populations (grant and bowen 1998 Aacuternason et al 2000 Aacuternason 2004) The shallow genealogies can be explained by coalescence theory that allows for multiple mergers in a genealogy (ie many individuals sharing a parent) or even simultaneous multiple mergers at a single time-step of the model (eldon and wakeley 2006 Sargsyan and wakeley 2008) Shallow genealogies can also be explained by population bottlenecks or selective sweeps but these appear not to be parsimonious explanations since bottlenecks or selective sweeps would have to have occurred in many marine species at a similar time and in marine species more often than in terrestrial species which typically do not show these star phylogenies

Mtdna sequences in the dabob bay population of pacific oysters which has a low NeN ratio (Hedgecock 1994a) and genetic differentiation among larval cohorts (li and Hedgecock 1998) show an extreme star phylogeny (Fig 4) as described by li and Hedgecock (1998) sequence variation was revealed as single-strand confor-mational polymorphisms (SScp) of eight fragments spanning 2281 bp of the mito-chondrial genome Subsequent sequencing of SScp variants for two fragments of the CYTB gene revealed that SScp variants represented unique sequences differing by one or two nucleotides from the common type which was essentially homogeneous at the sequence level (li and Hedgecock unpubl data) in addition to the 877 samples


reported by li and Hedgecock (1998) Figure 4 shows samples of spat from 1985 and 1994 and a sample of adults from 1995 a total of 1112 individuals The common eight-fragment SScp haplotype at the center of the graph is present in 769 indi-viduals 152 variants are distributed around the common sequence in decreasing frequency with degree of sequence distance from the common type (ie the number of SScp differences with a maximum of eight possible) The majority of variants despite being rare are shared among samples although turnover of rare variants is suggested by the absence from over 1000 individuals sampled 8ndash10 yrs later of five variants present in 1985 including one that is four SScp steps removed from the common type Aacuternason et al (2000) and Aacuternason (2004) came to similar conclusions about mtdna sequence diversity and turnover in cod

Thus the skewed frequency-profile of mtdna variants so commonly observed in marine animals with one or a few common haplotypes and many rare haplotypes may represent a dynamic equilibrium between a high rate of drift owing to SRS and a high rate of mutation which itself may be a by-product of the many germ-line cell divisions required for high fecundity in this regard the mutation effective size of a marine animal genealogy (sensu wakeley and Sargsyan 2009) may be more closely

Figure 4 A network of 153 mtDNA single-strand conformational polymorphisms (SSCP) found in the Dabob Bay oyster population The common type at the center is present in 769 of 1112 individuals Variants are arranged around the common type along concentric circles depicting degrees of separation (1˚ = one SSCP difference out of a maximum of eight) In the innermost circle the 1˚ variants are grouped into a sector shared by two or more samples and a sector found in only one sample (private) Variants in the outer circles connect to the most frequent variant with which they share k-1 changes from the common type Frequencies of 1˚ variants from which 2˚ variants derive are given at the base of each branch some ancestral sequences are not ob-served (question marks) Numbers of individuals and samples for variants of two or more degrees of separation appear at each branch tip Five haplotypes present in 1985 () including one of 4˚ separation are absent from over 1000 individuals sampled 8ndash10 yrs later (1993 larvae 1994 spat 1995 adults )


related to the number and genealogy of successful gametes than to the number and genealogy of adults

The effect of bottlenecks can be simulated for mtdna sequence diversity in the pacific oyster (table 1) Sequencing of all SScp variants and a large sample of the common SScp type for a 484 base-pair fragment of the mitochondrial CYTB gene identified 54 haplotypes among 744 individuals with 50 segregating sites but an av-erage pairwise difference among sequences of only 025 nucleotides since 665 indi-viduals have the most common haplotype (table 1) For the observed data tajimarsquos (1989a) D-test of neutrality is significantly negative meaning that relative to neu-tral evolution in a standard kingman coalescent there is an excess of segregating sites and singletons given the small differences among sequences in simulations of a population of 10 million individuals 10 thousand generations after a bottle-neck to a single sequence a similar level of D is reached only when a typical rate of mutation has created 263 segregating sites and the frequency of the ancestral hap-lotype has declined to 445 of 744 individuals Thus a single bottleneck is unlikely to be responsible for the observed pattern of CYTB sequence diversity a haplotype frequency-profile similar to that observed is obtained by simulating periodic bottle-necks However an alternative and perhaps more parsimonious explanation of the data is provided by SRS Sargsyan and wakeley (2008) showed that the mtdna hap-lotype frequency-profile obtained for dabob bay and british columbia populations of the pacific oyster (boom et al 1994) fit a coalescent model allowing for multiple mergers in the genealogy better than a coalescent allowing only for binary mergers of ancestral lines

The recent development of coalescent models appropriate for SRS is a major advance for marine population genetics which means however that estimating long-term Ne or migration rates using molecular data and kingman coalescent methods as has become popular in the literature may not be valid and may produce misleading results (wakeley and Sargsyan 2009) although sample sizes necessary for ruling out bifurcating ancestral genealogical processes when multifurcating genealogies are likely to have occurred need to be on the order of the number of breeders (wakeley and Sargsyan 2009) the very low NeN ratios that have been observed thus far for many marine species offer encouragement that adequate sample sizes are attainable

Table 1 Observed and simulated nucleotide polymorphism in a 484 bp fragment of the mitochondrial CYTB gene in a Pacific oyster population

Number first five haplotypes Statisticsa

A B C D E F hap S k DObserved nucleotide polymorphismb

665 7 4 3 3 3 54 50 025 minus260Simulated polymorphism after a single bottleneckc

455 3 3 3 3 2 263 238 104 minus283Simulated polymorphism with repeated bottlenecksd

669 6 3 3 3 3 52 50 021 minus261a hap number of haplotypes detected S number of segregating sites k average number of nucleotide differences between randomly chosen pairs of sequences D Tajimarsquos (1989a) test statistic which is expected to be zero at equilibrium but is significantly negative for the observed and simulated datab Based on 744 CYTB sequences from Dabob Bay Pacific oysters Crassostrea gigas c 10000 generations after a bottleneck to one sequence with Nb = 107 in all subsequent generations and μ = 10minus7

d 1681 generations after a bottleneck to one sequence followed by repeated bottlenecks of Nb = 2400 every 400 generations with Nb = 107 between bottlenecks and μ = 15 times 10minus7


More powerful tests of kingmanrsquos coalescent may also be afforded by use of multiple loci and examination of patterns of linkage disequilibrium (eldon and wakeley 2008)

discussion

Review of a database of literature on SRS reveals widespread support for the hypothesis despite difficulties in estimating N Ne and Nb or their ratios NeN and NbN (nunney 1996 palstra and Ruzzante 2008 waples 2005 luikart et al 2010) and despite the particular limitations in testing SRS predictions reviewed here substantial evidence exists for very low NeN ratios (ltlt 001) in highly fecund fishes including some freshwater species and marine invertebrates These very low NeN ratios which are mostly estimated in temporal studies are unlikely to be explained by methodological errors or publication bias SRS is corroborated moreover by numerous cohort analyses revealing low NbN ratios The conclusion is inescapable that SRS does occur The important questions that remain are to what extent how often where and why does SRS occur whether for example variance in reproductive success is spatial based on variability among spawning (park et al 1999) or nursery habitats (turner et al 2002) or is truly among individuals regardless of their location is critical to fisheries management and the design of marine reserves what is firmly established by this review nevertheless is the necessity of identifying not only spatial population structure (ward 2006) but also temporal population structure in the analysis and management of highly fecund fish and shellfish populations (Hedgecock et al 2007b)

before closing we discuss two misconceptions about SRS and highlight the implications of SRS for interpreting spatial structure and connectivity of marine populations

High fecundity does not cause SRSmdashnunney (1996) criticized the idea that ldquohigh fecundity predisposes a species to a high variance in reproductive success and hence to potentially low values of NeNrdquo based on theory that ldquothe effect of fecundity variation acts through its standardized variance [variance(mean)2] which is gen-erally independent of the meanrdquo and data from terrestrial animals (insects birds mammals) showing that this standardized variance is typically between 0 and 1 yet nunney conceded that loss of complete families (crow and Morton 1955 waples 2002) could lead to large variance in reproductive success and a reduction in the NeN ratio precisely what is envisioned by the SRS hypothesis High fecundity does not cause SRS but instead provides scope for variance in reproductive success which is determined by a chain of events extending from maturation to spawning fertiliza-tion larval survival settlement metamorphosis and recruitment to the adult popu-lation SRS occurs if and only if the environment induces differential reproduction contributions or family-correlated survival (waples 2002 turner et al 2006)

nunney (1996) speculated that an estimate of NeN = 10minus6 for dabob bay pacific oysters (Hedgecock et al 1992) was caused by mixing of farmed and wild oysters not drift However such speculation is at odds with the history of culture operations and larval production in dabob bay (see Hedgecock 1994a and references therein) Moreover an admixture explanation in this case cannot account for the dozens of other studies that have subsequently reported NeN ltlt 001 or for studies showing that cohorts have genetic signatures of being produced by a limited number of par-


ents what seems clear from the SRS literature is that reproductive success of highly fecund marine animals and some freshwater fishes cannot be inferred from studies of terrestrial animals which have much lower fecundities and type i or type ii sur-vival (clutton-brock 1988)

SRS at the cohort and Species levelsmdashSome authors find predicted signals of SRS in cohorts but doubt that the phenomenon is of much consequence for the population as a whole For example Selkoe et al (2006) state ldquoThe amount of ge-netic drift resulting from the observed frequency of sibships is not likely substantial enough to have a strong impact on adult genetic structure as it is averaged out across multiple cohorts that are subsumed into the year class of an entire recruitment sea-sonrdquo buston et al (2009) are even more forceful ldquoas with many problems in ecology and behavior evidence for the sweepstakes hypothesis will be contingent on spatial scale and the measure of reproductive success Here although there is a sweepstakes effect when lsquoproduction of offspringrsquo (small individuals) is used as the metric of re-productive success the effect apparently disappears when lsquoproduction of offspring that survive to breedrsquo (large individuals) is used as the metric of reproductive suc-cesshellipThat is to say that the sweepstakes effecthellipis an ecological phenomenon that seems to have no evolutionary consequencesrdquo

The genetic signals of SRS imprinted on cohorts particularly the weak genotypic signals of ld and relatedness are expected to be lost as cohorts accumulate and are incorporated into the adult population This is precisely what has long been observed for marine animal populations (Johnson et al 1982 1984 watts et al 1990 edmands et al 1996 Johnson and wernham 1999 Moberg and burton 2000 planes and lenfant 2002) The evolutionary consequences of SRS at the scale of populations and species on the other hand are clear and profound low genetic or dna-sequence diversity relative to population size low NeN ratio and thus much more random genetic drift and inbreeding than is expected based on the census number These large-scale consequences of SRS have been observed in a wide variety of marine animal taxa using methods other than those based on cohort analyses

likewise some may be troubled by use of data from a single cohort sampled at one location to support SRS at the level of the entire population while the con-sequences of SRS on the effective size of an entire population certainly cannot be tested by sampling a single cohort at a single locality the predictions that SRS makes about the genetics of cohorts are nevertheless worth testing The difference between temporal and cohort approaches to testing SRS is analogous to lagrangian and eu-lerian frames of reference in oceanography ie one can follow an adult (or larval) population over space and time (lagrangian) or one can sit in one spot and study what is recruiting locally (eulerian) each frame of reference is valid combined they provide for a powerful understanding of evolutionary change in marine populations The value of a cohort study is increased if the genetics of cohorts can be put into the context of spatial structure among adult populations in the case of the flat oyster adult populations were known to be homogeneous throughout the Mediterranean Sea (launey et al 2002) thus eliminating some alternative explanations at least for some aspects of the cohort data (Hedgecock et al 2007b) such as delivery of larvae from a differentiated source populations a challenge for future research is to inte-grate the testing of SRS predictions across both adult-population and cohort stages as exemplified by christie et al (2010 Hedgecock 2010)


interpretation of Spatial variation in Marine Species under SRSmdashin light of the considerable evidence for temporal genetic structure of marine animal populations the simple idea that ldquoone may interpret genetic differentiation among populations in terms of population isolation reduced gene flow genetic drift and natural selectionrdquo (gonzaacutelez-wanguumlemert et al 2007) is no longer tenable Rightly gonzaacutelez-wanguumlemert et al (2007) went on to state ldquohellipquestions often arise regard-ing the biological significance of such differentiation partly since the temporal sta-bility of the observed pattern is unknown (waples 1998)rdquo unfortunately waplesrsquo (1998) caution about the need to observe temporal stability of spatial patterns before inferring barriers to gene flow has not been universally heeded temporal stability of geographical structure has been observed in some cases though not necessarily to the exclusion of temporal change within sub-populations bernal-Ramirez et al (2003) showed that the new Zealand snapper Chrysophrys auratus (Foster in block and Schneider 1801) had a temporally stable population structure over decades de-spite evidence for genetic drift within the heavily fished tasman bay stock (Hauser et al 2002) larsson et al (2010) demonstrated stability of weak genetic differentiation of baltic and Skagerrak herring stocks over two decades despite evidence for genetic drift and finite Ne within stocks (~1600 for Skagerrak samples and ~2100 for baltic samples) and noted how few studies have confirmed the temporal stability of spatial structure For species with overlapping generations three to five generations or more of separation between temporal samples may be needed to confirm or falsify stability (waples and yakota 2007) Such a standard has rarely been met in marine popula-tion genetics to put the standard in practical perspective a four-generation interval to show stability given mean generation times of five or more years for marine fish (winemiller and Rose 1992) is nearly 10 times longer than the typical research grant in some cases archived tissues or scales enable genetic study of past generations as demonstrated by the papers cited above

The development of coalescent population genetic theory that accounts for SRS has brought the difficulty of interpreting spatial genetic variation into sharp focus esti-mates of FST can be non-zero and significant even when gene flow is very high be-cause variance in reproductive success contributes to variance in allelic frequencies among populations (eldon and wakeley 2009) in other words SRS itself can gener-ate the sort of transitory small-scale spatial variation or ldquochaotic patchinessrdquo that has typically been observed in marine populations with global FST lt 0001 (Hauser and carvalho 2008) This aspect of SRS is illustrated in Fig 5 which shows a single time-step of reproduction for a finite haploid (eg mtdna) coastal marine animal population with overlapping generations (after Sargsyan and wakeley 2008) with such a small number of individuals this figure cannot illustrate a variance in repro-ductive success as large as that required for SRS but the figure does illustrate how ldquochaotic patchinessrdquo can arise

one implication of this theoretical advance is that estimating larval flux or the absolute number of migrants Nm from Sewell wrightrsquos classical formula FST = 1 (4Nm + 1) is no longer acceptablemdashif it ever was following whitlock and Mccauleyrsquos (1999) emphatically titled article a more positive implication for marine science is that genetic analysis of larval cohorts with sufficiently rigorous sampling could well shed light on larval dispersal kernels precisely because SRS can impart a characteristic genetic profile on a larval cohort which can then be tracked in space and time However to carry out genetic studies of cohorts with a lagrangian frame


of reference (cf Siegel et al 2003) will likely require a scale of sampling that has rarely if ever been achieved in marine population genetics

conclusions and Future directions

natural populations of marine animals have a suite of life-history traits that makes them dramatically different from most terrestrial animals especially the model spe-cies for which reproductive success is well described (clutton-brock 1988) and on which most traditional population genetic theory is founded (eg nunney 1996) Most marine animals evolved as very abundant long-lived late-maturing and highly fecund adults adapted to spatially and temporally fluctuating ocean environ-ments (winemuller and Rose 1992) adults typically produce millions of small eggs that develop rapidly without parental care into ecologically distinct small weakly swimming larval stages that disperse widely but suffer high early mortality (type iii survivorship) The interaction of high fecundity and high mortality in a temporally and spatially patchy planktonic environment results in high variance in reproduc-

Figure 5 A haploid model of Sweepstakes Reproductive Success in a finite coastal marine ani-mal population with overlapping generations (after Sargsyan and Wakeley 2008) A single time-step of reproduction is shown At time t

1 there are individuals that reproduce successfully (three

filled ovals) individuals that fail to reproduce (nine gray-centered ovals) and individuals that fail to reproduce but persist to t

2 (eight unfilled ovals) At time t

2 there are the individuals that

persisted from t1 (unfilled and filled ovals fine dotted connections back to t

1) and new recruits

(filled parallelograms heavier parent-specific connection lines back to t1) With a population size

of only 20 in this illustration variance in reproductive success is orders of magnitude too small for SRS However the illustration does show the transitory spatial genetic structure (ldquochaotic patchinessrdquo) that is expected to arise when the offspring of reproductively successful adults do not disperse across the whole range in a single time-step


tive success Marine population genetics has to account for this high variance in reproductive success and we have reviewed various approaches for doing that Si-multaneous application of multiple approaches at different time-scales [evolutionary temporal (multi-generational) and cohort] should help to diminish the risk that a study is done at a time when environmental conditions promoting SRS might not exist use of multiple loci in all approaches can help to disentangle selective vs de-mographic forces

The hypothesis of SRS explains many widespread observations that have been made on the genetics of marine animal populations (1) shallow genealogies and star phylogenies of mtdna sequences (2) levels of molecular genetic diversity that are much lower than expected given enormous census sizes (3) transient ldquochaoticrdquo ge-netic patchiness which occurs on small spatial scales despite homogeneity or great similarity of adult populations on broad spatial scales and which is related to site-specific recruitment history (4) random genetic drift in natural populations that gives rise to estimates of small effective population sizes and low NeN ratios (ltlt 001) and (5) cohorts of recruits that are not in random-mating equilibrium some-times show evidence of kinship and are more different from one another and from adult populations than adult populations are from each other to this list could be added the widespread observations particularly for bivalve molluscs of positive cor-relation between allozyme heterozygosity and fitness-related traits such as growth and survival (gaffney 1994 Zouros and pogson 1994) which can be explained by a combination of gametic-phase disequilibrium induced in recruiting cohorts by SRS and a large load of recessive deleterious mutations (david et al 1997 bierne et al 1998 launey and Hedgecock 2001)

The broad explanatory power of the SRS hypothesis does not immunize it against falsification or exclude alternative explanations for some observations there may well be real barriers to larval dispersal resulting in temporally stable spatial structure historical bottlenecks in population size or natural selection SRS is probably not the best explanation for example for low NeN ratio in the thornback ray (chevolot et al 2008) or in small moderately fecund pelagic fishes that undergo dramatic fluctuations in abundance (grant and bowen 1998) However SRS does offer a unifying parsimonious explanation for the genetic characteristics of marine populations and provides a tractable selectively neutral null hypothesis against which to test hypotheses regarding larval flux or natural selection

SRS appears to occur in a wide variety of taxa and is thus worthy of consider-ation in every genetic study of marine animals just as spatial genetic variation is now routinely considered Spatial population structure cannot be taken as evidence for oceanographic restrictions to larval dispersal unless there is sufficient data to con-clude that the spatial pattern is stable over several generations and that confound-ing effects of SRS and temporal environmental variation have been taken fully into account on the other hand direct genetic approaches to estimating Nb for cohorts and use of genetics in studies that track specific larval cohorts in part by their SRS-induced genetic profiles hold tremendous promise for gaining insight into marine biological processes The biological basis of SRS starting from adult spawning and fertilization success (park et al 1999 berkeley et al 2004 levitan 2005 lowerre-barbieri et al 2009) and running through larval survival and dispersal (cushing 1990 cowen et al 2006 2007) to post-recruitment success (pineda et al 2007) needs much more study Finally the gap between theory and practice in marine popula-


tion genetics which is revealed here by citation analysis needs to be bridged co-alescent models allowing multifurcating rather than strictly bifurcating genealogical processes need to be used to estimate demographic and evolutionary parameters from nuclear and mtdna sequences development of statistical tools to help decide among competing coalescent models and to draw inferences about demographic and genetic parameters of interest is welcome (eg birkner and blath 2008)

in this review we have intentionally excluded studies of cultured populations but a large literature supports the notion that Vk is high in most hatchery populations of highly fecund fish and shellfish High Vk and rapid genetic drift in hatchery propa-gated populations have implications for maintenance of genetic diversity in cultured stocks or wild stocks that are supplemented with hatchery-propagated seed and for interaction of farmed and wild stocks (Hedgecock and coykendall 2007)

acknowledgments

we thank e garfield for allowing us to use Histcite we are indebted also to R waples and two anonymous reviewers for many insightful comments and suggestions on earlier drafts

literature cited

alo d turner tF 2005 effects of habitat fragmentation on effective population size in the endangered Rio grande silvery minnow conserv biol 191138ndash1148 httpdxdoiorg101111j1523-1739200500081x

ammann aJ 2004 SMuRFs standard monitoring units for the recruitment of temperate reef fishes J exp Mar biol ecol 299135ndash154 httpdxdoiorg101016jjembe200308014

Aacuternason e 2004 Mitochondrial cytochrome b dna variation in the high-fecundity atlantic cod trans-atlantic clines and shallow gene genealogy genetics 1661871ndash1885 pMid15126405 pMcid1470818 httpdxdoiorg101534genetics16641871

Aacuternason e petersen pH kristinsson k Sigurgislason H palsson S 2000 Mitochondrial cytochrome b dna sequence variation of atlantic cod from iceland and greenland J Fish biol 56409ndash430

avise Jc 1994 Molecular Markers natural History and evolution new york chapman amp Hall

avise Jc ball RM arnold J 1988 current versus historical population sizes in vertebrate species with high gene flow a comparison based on mitochondrial dna lineages and inbreeding theory for neutral mutations Mol biol evol 5331ndash344 pMid3405076

ball ao chapman Rw 2003 population genetic analysis of white shrimp Litopenaeus setiferus using microsatellite genetic markers Mol ecol 122319ndash2330 pMid12919471 httpdxdoiorg101046j1365-294X200301922x

barcia aR lopez ge Hernandez d garcia-Machado e 2005 temporal variation of the population structure and genetic diversity of Farfantepenaeus notialis assessed by allozyme loci Mol ecol 142933ndash2942 pMid16101764 httpdxdoiorg101111j1365-294X200502613x

beckenbach at 1994 Mitochondrial haplotype frequencies in oysters neutral alternatives to selection models In golding b editor non-neutral evolution theories and molecular data new york chapman amp Hall p 188ndash198

bekkevold d Hansen MM loeschcke v 2002 Male reproductive competition in spawning aggregations of cod (Gadus morhua l) Mol ecol 1191ndash102 pMid11903907 httpdxdoiorg101046j0962-1083200101424x


bentzen p taggart ct Ruzzante de cook d 1996 Microsatellite polymorphism and the population structure of atlantic cod (Gadus morhua) in the northwest atlantic can J Fish aquat Sci 532706ndash2721 httpdxdoiorg101139cjfas-53-12-2706

benzie JaH Frusher S ballment e 1992 geographical variation in allozyme frequencies of populations of Penaeus monodon (crustacea decapoda) in australia aust J Mar Freshwat Res 43715ndash725 httpdxdoiorg101071MF9920715

berestycki J berestycki n limic v 2010 The Λ-coalescent speed of coming down from infinity ann prob 38207ndash233 httpdxdoiorg10121409-aop475

berger eM 1973 gene-enzyme variation in three sympatric species of Littorina biol bull 14583ndash90 httpdxdoiorg1023071540349

berkeley Sa Hixon Ma larson RJ love MS 2004 Fisheries sustainability via protection of age structure and spatial distribution of fish populations Fisheries 2923ndash32 httpdxdoiorg1015771548-8446(2004)29[23FSvpoa]20co2

bernal-Ramirez JH adcock gJ Hauser l carvalho gR Smith pJ 2003 temporal stability of genetic population structure in the new Zealand snapper Pagrus auratus and relationship to coastal currents Mar biol 142567ndash574

berthier p beaumont Ma cornuet JM luikart g 2002 likelihood-based estimation of the effective population size using temporal changes in allele frequencies a genealogical approach genetics 160741ndash751 pMid11861575 pMcid1461962

bierne n launey S naciri-graven y bonhomme F 1998 early effect of inbreeding as revealed by microsatellite analyses on Ostrea edulis larvae genetics 1481893ndash1906 pMid9560403 pMcid1460075

birkner M blath J 2008 computing likelihoods for coalescents with multiple collisions in the infinitely many sites model J Math biol 57435ndash465 pMid18347796 httpdxdoiorg101007s00285-008-0170-6

bohonak aJ 1999 dispersal gene flow and population structure Quart Rev biol 7421ndash45 pMid10081813 httpdxdoiorg101086392950

boom Jdc boulding eg beckenbach at 1994 Mitochondrial dna variation in introduced populations of pacific oyster Crassostrea gigas in british columbia can J Fish aquat Sci 511608ndash1614 httpdxdoiorg101139f94-160

borrell yJ arenal F Mbemba ZM Santana o diaz-Fernandez R vazquez e blanco g Sanchez Ja espinosa g 2007 Spatial and temporal genetic analysis of the cuban white shrimp Penaeus (Litopenaeus) schmitti aquaculture 272S125ndashS138 httpdxdoiorg101016jaquaculture200708015

boudry p collet b cornette F Hervouet v bonhomme F 2002 High variance in reproductive success of the pacific oyster (Crassostrea gigas Thunberg) revealed by microsatellite-based parentage analysis of multifactorial crosses aquaculture 204283ndash296 httpdxdoiorg101016S0044-8486(01)00841-9

bucklin ka banks Ma Hedgecock d 2009 assessing genetic diversity of protected coho salmon populations (Oncorhynchus kisutch) in california can J Fish aquat Sci 6430ndash42 httpdxdoiorg101139F06-171

burford Mo larson RJ 2007 genetic heterogeneity in a single year class from a panmictic population of adult blue rockfish (Sebastes mystinus) Mar biol 151451ndash465 httpdxdoiorg101007s00227-006-0475-1

burton RS 1983 protein polymorphisms and genetic differentiation of marine invertebrate populations Mar biol lett 4193ndash206

buston pM Fauvelot c wong Myl planes S 2009 genetic relatedness in groups of the humbug damselfish Dascyllus aruanus small similar-sized individuals may be close kin Mol ecol 184707ndash4715 pMid19845858 httpdxdoiorg101111j1365-294X200904383x

calderoacuten i palacin c turon X 2009 Microsatellite markers reveal shallow genetic differentiation between cohorts of the common sea urchin Paracentrotus lividus (lamarck) in northwest Mediterranean Mol ecol 183036ndash3049 pMid19500246 httpdxdoiorg101111j1365-294X200904239x


cassista Mc Hart Mw 2007 Spatial and temporal genetic homogeneity in the arctic surfclam (Mactromeris polynyma) Mar biol 152569ndash579 httpdxdoiorg101007s00227-007-0711-3

chevolot M ellis JR Rijnsdorp ad Stam wt olsen Jl 2008 temporal changes in allele frequencies but stable genetic diversity over the past 40 years in the irish Sea population of thornback ray Raja clavata Heredity 101120ndash126 pMid18461082 httpdxdoiorg101038hdy200836

christie MR Johnson dw Stallings cd Hixon Ma 2010 Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish Mol ecol 191042ndash1057 pMid20089121 httpdxdoiorg101111j1365-294X201004524x

clutton-brock tH 1988 Reproductive Success chicago university of chicago presscowen Rk paris cb Srinivasan a 2006 Scaling of connectivity in marine populations

Science 311522ndash527 pMid16357224 httpdxdoiorg101126science1122039cowen Rk gawarkiewicz g pineda J Thorrold SR werner Fe 2007 population connectivity

in marine systems an overview oceanography 2014ndash20crow JF Morton ne 1955 Measurement of gene frequency drift in small populations

evolution 9202ndash21424crow JF denniston c 1988 inbreeding and variance effective population numbers evolution

42482ndash495 httpdxdoiorg1023072409033cushing dH 1990 plankton production and year-class strength in fish populations an update

of the MatchMismatch Hypothesis adv Mar biol 26249ndash293 httpdxdoiorg101016S0065-2881(08)60202-3

dannewitz J Maes ge Johansson l wickstrom H volckaert FaM Jarvi t 2005 panmixia in the european eel a matter of timehellip proc Roy Soc b 2721129ndash1137 pMid16024374 pMcid1559815 httpdxdoiorg101098rspb20053064

david p perdieu M-a pernot a-F Jarne p 1997 Fine-grained spatial and temporal population genetic structure in the marine bivalve Spisula ovalis evolution 511318ndash1322 httpdxdoiorg1023072411061

demandt MH 2010 temporal changes in genetic diversity of isolated populations of perch and roach conserv genet 11249ndash255 httpdxdoiorg101007s10592-009-0027-6

edmands S Moberg pe burton RS 1996 allozyme and mitochondrial dna evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus Mar biol 126443ndash450 httpdxdoiorg101007bF00354626

eldon b 2009 Structured coalescent processes from a modified Moran model with large offspring numbers Theo pop biol 7692ndash104 pMid19433101 httpdxdoiorg101016jtpb200905001

eldon b wakeley J 2006 coalescent processes when the distribution of offspring number among individuals is highly skewed genetics 1722621ndash2633 pMid16452141 pMcid1456405 httpdxdoiorg101534genetics105052175

eldon b wakeley J 2008 linkage disequilibrium under skewed offspring distribution among individuals in a population genetics 1781517ndash1532 pMid18245371 pMcid2278056 httpdxdoiorg101534genetics107075200

eldon b wakeley J 2009 coalescence times and FSt under a skewed offspring distribution among individuals in a population genetics 181615ndash629 pMid19047415 pMcid2644951 httpdxdoiorg101534genetics108094342

Flowers JM Schroeter Sc burton RS 2002 The recruitment sweepstakes has many winners genetic evidence from the sea urchin Strongylocentrotus purpuratus evolution 561445ndash1453 pMid12206244

Frankham R 1995 effective population sizeadult population size ratios in wildlife a review genet Res 6695ndash107 httpdxdoiorg101017S0016672300034455

gaffney pM 1994 Heterosis and heterozygote deficiencies in marine bivalves more light In beaumont a editor genetics and evolution of aquatic organisms london chapman amp Hall p 146ndash153


gaffney pM davis cv Hawes Ro 1992 assessment of drift and selection in hatchery populations of oysters (Crassostrea virginica) aquaculture 1051ndash20 httpdxdoiorg1010160044-8486(92)90157-g

garfield e pudovkin ai istomin vS 2002 algorithmic citation-linked historiographymdashmapping the literature of science proc aSiSt ann Meeting 3914ndash24

garfield e pudovkin ai istomin vS 2003 why do we need algorithmic historiography J am Soc inf Sci tec 54400ndash412 httpdxdoiorg101002asi10226

goodnight kF Queller dc 1999 computer software for performing likelihood tests of pedigree relationship using genetic markers Mol ecol 81231ndash1234 httpdxdoiorg101046j1365-294x199900664x

gonzaacutelez-wanguumlemert n perez-Ruzafa a canovas F garcia-charton Ja Marcos c 2007 temporal genetic variation in populations of Diplodus sargus from the Sw Mediterranean Sea Mar ecol prog Ser 334237ndash244 httpdxdoiorg103354meps334237

gosling eM wilkins np 1985 genetics of settling cohorts of Mytilus edulis (l)mdashpreliminary observations aquaculture 44115ndash123 httpdxdoiorg1010160044-8486(85)90014-6

grant wS bowen bw 1998 Shallow population histories in deep evolutionary lineages of marine fishes insights from sardines and anchovies and lessons for conservation J Hered 89415ndash426 httpdxdoiorg101093jhered895415

gyllensten u 1985 The genetic-structure of fishmdashdifferences in the intraspecific distribution of biochemical genetic-variation between marine anadromous and fresh-water species J Fish biol 26691ndash699 httpdxdoiorg101111j1095-86491985tb04309x

Han yS Sun yl liao yF liao ic Shen kn tzeng wn 2008 temporal analysis of population genetic composition in the overexploited Japanese eel Anguilla japonica Mar biol 155613ndash621 httpdxdoiorg101007s00227-008-1057-1

Han yS Hung cl liao yF tzeng wn 2010 population genetic structure of the Japanese eel Anguilla japonica panmixia at spatial and temporal scales Mar ecol prog Ser 401221ndash232 httpdxdoiorg103354meps08422

Hauser l carvalho gR 2008 paradigm shifts in marine fisheries genetics ugly hypotheses slain by beautiful facts Fish Fish 9333ndash362 httpdxdoiorg101111j1467-2979200800299x

Hauser l adcock gJ Smith pJ Ramirez JHb carvalho gR 2002 loss of microsatellite diversity and low effective population size in an overexploited population of new Zealand snapper (Pagrus auratus) proc nat acad Sci uSa 9911742ndash11747 pMid12185245 pMcid129339 httpdxdoiorg101073pnas172242899

Hedgecock d 1982 genetic consequences of larval retention theoretical and methodological aspects In kennedy vS editor estuarine comparisons new york academic press p 553ndash568

Hedgecock d 1986 is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates bull Mar Sci 39550ndash564

Hedgecock d 1994a does variance in reproductive success limit effective population size of marine organisms In beaumont a editor genetics and evolution of aquatic organisms london chapman amp Hall p 122ndash134

Hedgecock d 1994b temporal and spatial genetic-structure of marine animal populations in the california current cal coop oceanic Fish invest Reports 3573ndash81

Hedgecock d 2010 determining parentage and relatedness from genetic markers sheds light on patterns of marine larval dispersal Mol ecol 19845ndash847 pMid20456220 httpdxdoiorg101111j1365-294X201004525x

Hedgecock d barber pH edmands S 2007a genetic approaches to measuring connectivity oceanography 2070ndash79

Hedgecock d coykendall k 2007 genetic risks of hatchery enhancement the good the bad and the unknown In bert tM editor ecological and genetic implications of aquaculture activities dordrecht Springer p 85ndash101 httpdxdoiorg101007978-1-4020-6148-6_5


Hedgecock d chow v waples RS 1992 effective population numbers of shellfish broodstocks estimated from temporal variance in allelic frequencies aquaculture 108215ndash232 httpdxdoiorg1010160044-8486(92)90108-w

Hedgecock d launey S pudovkin ai naciri y lapegue S bonhomme F 2007b Small effective number of parents (nb) inferred for a naturally spawned cohort of juvenile european flat oysters Ostrea edulis Mar biol 1501173ndash1182 httpdxdoiorg101007s00227-006-0441-y

Hedgecock d Sly F 1990 genetic drift and effective population sizes of hatchery-propagated stocks of the pacific oyster Crassostrea gigas aquaculture 8821ndash38 httpdxdoiorg1010160044-8486(90)90316-F

Hedgecock d tracey Ml nelson k 1982 genetics In abele lg editor The biology of crustacea vol 2 new york academic press p 297ndash403

Hedrick p 2005 large variance in reproductive success and the nen ratio evolution 591596ndash1599 pMid16153045

Hellberg Me 2009 gene flow and isolation among populations of marine animals ann Rev ecol evol Syst 40291ndash310 httpdxdoiorg101146annurevecolsys110308120223

Hellberg Me burton RS neigel Je palumbi SR 2002 genetic assessment of connectivity among marine populations bull Mar Sci 70273ndash290

Hepburn Ri Sale pF dixon b Heath dd 2009 genetic structure of juvenile cohorts of bicolor damselfish (Stegastes partitus) along the Mesoamerican barrier reef chaos through time coral Reefs 28277ndash288 httpdxdoiorg101007s00338-008-0423-2

Herbinger cM doyle Rw taggart ct lochmann Se brooker al wright JM cook d 1997 Family relationships and effective population size in a natural cohort of atlantic cod (Gadus morhua) larvae can J Fish aquat Sci 54 (Suppl 1)11ndash18 httpdxdoiorg101139cjfas-54-S1-11

Hill wg 1981 estimation of effective population size from data on linkage disequilibrium genet Res 38209ndash216 httpdxdoiorg101017S0016672300020553

Hjort J 1914 Fluctuations in the great fisheries of northern europe viewed in the light of biological research Rapp procs-verb Reun cons int explor Mer 201ndash228

Hoarau g boon e Jongma dn Ferber S palsson J van der veer Hw Rijnsdorp ad Stam wt olsen Jl 2005 low effective population size and evidence for inbreeding in an overexploited flatfish plaice (Pleuronectes platessa l) proc Roy Soc b 272497ndash503 pMid15799945 pMcid1578705 httpdxdoiorg101098rspb20042963

Johnson MS black R 1982 chaotic genetic patchiness in an intertidal limpet Siphonaria sp Mar biol 70157ndash164 httpdxdoiorg101007bF00397680

Johnson MS black R 1984 pattern beneath the chaos the effect of recruitment on genetic patchiness in an intertidal limpet evolution 381371ndash1383 httpdxdoiorg1023072408642

Johnson MS wernham J 1999 temporal variation of recruits as a basis of ephemeral genetic heterogeneity in the western rock lobster Panulirus cygnus Mar biol 135133ndash139 httpdxdoiorg101007s002270050610

Jorde pe Ryman n 1995 temporal allele frequency change and estimation of effective size in populations with overlapping generations genetics 1391077ndash1090 pMid7713410 pMcid1206358

Jorde pe Ryman n 1996 demographic genetics of brown trout (Salmo trutta) and estimation of effective population size from temporal change of allele frequencies genetics 1431369ndash1381 pMid8807308 pMcid1207405

Jorde pe Ryman n 2007 unbiased estimator for genetic drift and effective population size genetics 177927ndash935 pMid17720927 pMcid2034655 httpdxdoiorg101534genetics107075481

kalinowski St 2004 counting alleles with rarefaction private alleles and hierarchical sampling designs conserv genet 5539ndash543 httpdxdoiorg101023bcoge0000041021917771a


koehn Rk newell Rie immermann F 1980 Maintenance of an aminopeptidase allele frequency cline by natural selection proc nat acad Sci uSa 775385ndash5389 httpdxdoiorg101073pnas7795385

kordos lM burton RS 1993 genetic differentiation of texas gulf-coast populations of the blue-crab Callinectes sapidus Mar biol 117227ndash233 httpdxdoiorg101007bF00345667

krimbas cb tsakas S 1971 The genetics of Dacus oleae v changes of esterase polymorphism in a natural population following insecticide controlmdashselection or drift evolution 25454ndash460 httpdxdoiorg1023072407343

larsson lc laikre l andre c dahlgren tg Ryman n 2010 temporally stable genetic structure of heavily exploited atlantic herring (Clupea harengus) in Swedish waters Heredity 10440ndash51 pMid19654606 httpdxdoiorg101038hdy200998

launey S Hedgecock d 2001 High genetic load in the pacific oyster Crassostrea gigas genetics 159255ndash265 pMid11560902 pMcid1461778

launey S ledu c boudry p bonhomme F naciri-graven y 2002 geographic structure in the european flat oyster (Ostrea edulis l) as revealed by microsatellite polymorphism J Hered 93331ndash338 pMid12547921 httpdxdoiorg101093jhered935331

leberg pl 2002 estimating allelic richness effects of sample size and bottlenecks Mol ecol 112445ndash2449 httpdxdoiorg101046j1365-294X200201612x

lee HJ boulding eg 2007 Mitochondrial dna variation in space and time in the northeastern pacific gastropod Littorina keenae Mol ecol 163084ndash3103 pMid17651189 httpdxdoiorg101111j1365-294X200703364x

lee HJ boulding eg 2009 Spatial and temporal population genetic structure of four northeastern pacific littorinid gastropods the effect of mode of larval development on variation at one mitochondrial and two nuclear dna markers Mol ecol 182165ndash2184 pMid19344352 httpdxdoiorg101111j1365-294X200904169x

lenfant p planes S 2002 temporal genetic changes between cohorts in a natural population of a marine fish Diplodus sargus biol J lin Soc 769ndash20 httpdxdoiorg101111j1095-83122002tb01710x

levitan dR 2005 The distribution of male and female reproductive success in a broadcast spawning marine invertebrate integr comp biol 45848ndash855 httpdxdoiorg101093icb455848

lewontin Rc krakauer J 1975 testing heterogeneity of F-values genetics 80397ndash398 pMid1132692 pMcid1213337

li g Hedgecock d 1998 genetic heterogeneity detected by pcR-SScp among samples of larval pacific oysters (Crassostrea gigas) supports the hypothesis of large variance in reproductive success can J Fish aquat Sci 551025ndash1033 httpdxdoiorg101139cjfas-55-4-1025

liu J-X ely b 2009 Sibship reconstruction demonstrates the extremely low effective population size of striped bass Morone saxatilis in the Santeendashcooper system South carolina uSa Mol ecol 184112ndash4120 pMid19735452 httpdxdoiorg101111j1365-294X200904343x

lowerre-barbieri Sk Henderson n llopiz J walters S bickford J Muller R 2009 defining a spawning population (spotted seatrout Cynoscion nebulosus) over temporal spatial and demographic scales Mar ecol prog Ser 394231ndash245 httpdxdoiorg103354meps08262

luikart g cornuet JM 1999 estimating the effective number of breeders from heterozygote excess in progeny genetics 1511211ndash1216 pMid10049936 pMcid1460520

luikart g Ryman n tallmon da Schwartz Mk allendorf Fw 2010 estimation of census and effective population sizes the increasing usefulness of dna-based approaches conserv genet 11355ndash373 httpdxdoiorg101007s10592-010-0050-7

lundy cJ Rico c Hewitt gM 2000 temporal and spatial genetic variation in spawning grounds of european hake (Merluccius merluccius) in the bay of biscay Mol ecol 92067ndash2079 pMid11123619 httpdxdoiorg101046j1365-294X200001120x


Maes ge pujolar JM Hellemans b volckaert FaM 2006 evidence for isolation by time in the european eel (Anguilla anguilla l) Mol ecol 152095ndash2107 pMid16780427 httpdxdoiorg101111j1365-294X200602925x

Marino iaM barbisan F gennari M giomi F beltramini M bisol pM Zane l 2010 genetic heterogeneity in populations of the Mediterranean shore crab Carcinus aestuarii (decapoda portunidae) from the venice lagoon estuar coast Shelf Sci 87135ndash144 httpdxdoiorg101016jecss201001003

Milkman R koehn Rk 1977 temporal variation in relationship between size numbers and an allele-frequency in a population of Mytilus edulis evolution 31103ndash115 httpdxdoiorg1023072407549

Moberg pe burton RS 2000 genetic heterogeneity among adult and recruit red sea urchins Strongylocentrotus franciscanus Mar biol 136773ndash784 httpdxdoiorg101007s002270000281

Mohle M 2006 on the number of segregating sites for populations with large family sizes adv appl probab 38750ndash767 httpdxdoiorg101239aap1158685000

Murray Mc Hare Mp 2006 a genomic scan for divergent selection in a secondary contact zone between atlantic and gulf of Mexico oysters Crassostrea virginica Mol ecol 154229ndash4242 pMid17054515 httpdxdoiorg101111j1365-294X200603060x

nei M graur d 1984 extent of protein polymorphism and the neutral mutation theory evol biol 1773ndash118

nei M Maruyama t chakraborty R 1974 bottleneck effect and genetic variability in populations evolution 291ndash10 httpdxdoiorg1023072407137

nei M tajima F 1981 genetic drift and estimation of effective population size genetics 98625ndash640 pMid17249104 pMcid1214463

ng wc leung Fcc chak Stc Slingsby g williams ga 2010 temporal genetic variation in populations of the limpet Cellana grata from Hong kong shores Mar biol 157325ndash337 httpdxdoiorg101007s00227-009-1320-0

nunney l 1996 The influence of variation in female fecundity on effective population size biol J lin Soc 59411ndash425 httpdxdoiorg101111j1095-83121996tb01474x

olsen Jb lewis cJ kretschmer eJ wilson Sl Seeb Je 2002 characterization of 14 tetranucleotide microsatellite loci derived from pacific herring Mol ecol notes 2101ndash103 httpdxdoiorg101046j1471-8286200200160x

osborne MJ benavides Ma turner tF 2005 genetic heterogeneity among pelagic egg samples and variance in reproductive success in an endangered freshwater fish Hybognathus amarus (cyprinidae) env biol Fish 73463ndash472 httpdxdoiorg101007s10641-005-3215-3

ovenden JR peel d Street R courtney aJ Hoyle Sd peel Sl podlich H 2007 The genetic effective and adult census size of an australian population of tiger prawns (Penaeus esculentus) Mol ecol 16127ndash138 pMid17181726 httpdxdoiorg101111j1365-294X200603132x

palm S dannewitz J prestegaard t wickstrom H 2009 panmixia in european eel revisited no genetic difference between maturing adults from southern and northern europe Heredity 10382ndash89 pMid19417764 httpdxdoiorg101038hdy200951

paacutelsson S kaumlllman t paulsen J Aacuternasson e 2009 an assessment of mitochondrial variation in arctic gadoids polar biol 32471ndash479 httpdxdoiorg101007s00300-008-0542-9

palstra Fp Ruzzante de 2008 genetic estimates of contemporary effective population size what can they tell us about the importance of genetic stochasticity for wild population persistence Mol ecol 173428ndash3447 httpdxdoiorg101111j1365-294X200803842x

palumbi SR wilson ac 1990 Mitochondrial dna diversity in the sea-urchins Strongylocentrotus purpuratus and Strongylocentrotus droebachiensis evolution 44403ndash415 httpdxdoiorg1023072409417

palumbi SR 1994 genetic divergence reproductive isolation and marine speciation ann Rev ecol Syst 25547ndash572 httpdxdoiorg101146annureves25110194002555


papetti c Susana e patarnello t Zane l 2009 Spatial and temporal boundaries to gene flow between Chaenocephalus aceratus populations at South orkney and South Shetlands Mar ecol prog Ser 376269ndash281 httpdxdoiorg103354meps07831

park MS lim HJ Jo Q yoo JS Jeon M 1999 assessment of reproductive health in the wild seed oysters Crassostrea gigas from two locations in korea J Shellfish Res 18445ndash450

pineda J Hare Ja Sponaugle S 2007 larval transport and dispersal in the coastal ocean and consequences for population connectivity oceanography 2022ndash39

planes S lecaillon g lenfant p Meekan M 2002 genetic and demographic variation in new recruits of Naso unicornis J Fish biol 611033ndash1049 httpdxdoiorg101111j1095-86492002tb01861x

planes S lenfant p 2002 temporal change in the genetic structure between and within cohorts of a marine fish Diplodus sargus induced by a large variance in individual reproductive success Mol ecol 111515ndash1524 pMid12144670 httpdxdoiorg101046j1365-294X200201521x

pollak e 1983 a new method for estimating the effective population size from allele frequency changes genetics 104531ndash548 pMid17246147 pMcid1202093

portnoy dS Mcdowell JR Mccandless ct Musick Ja graves Je 2009 effective size closely approximates the census size in the heavily exploited western atlantic population of the sandbar shark Carcharhinus plumbeus conserv genet 101697ndash1705 httpdxdoiorg101007s10592-008-9771-2

pudovkin ai Zaykin dv Hedgecock d 1996 on the potential for estimating the effective number of breeders from heterozygote-excess in progeny genetics 144383ndash387 pMid8878701 pMcid1207510

pudovkin ai Zhdanova ol Hedgecock d 2010 Sampling properties of the heterozygoteexcess estimator of the effective number of breeders conserv genet 11759ndash771 httpdxdoiorg101007s10592-009-9865-5

pujolar JM Maes ge volckaert FaM 2006 genetic patchiness among recruits in the european eel Anguilla anguilla Mar ecol prog Ser 307209ndash217 httpdxdoiorg103354meps307209

pujolar JM de leo ga ciccotti e Zane l 2009 genetic composition of atlantic and Mediterranean recruits of european eel Anguilla anguilla based on eSt-linked microsatellite loci J Fish biol 742034ndash2046 pMid20735687 httpdxdoiorg101111j1095-8649200902267x

pumitinsee p Senanan w na-nakorn u kamonrat w koedprang w 2009 temporal genetic heterogeneity of juvenile orange-spotted grouper (Epinephelus coioides pisces Serranidae) aquac Res 401111ndash1122 httpdxdoiorg101111j1365-2109200902206x

Rowe S Hutchings Ja Skjaeraasen Je bezanson l 2008 Morphological and behavioural correlates of reproductive success in atlantic cod Gadus morhua Mar ecol prog Ser 354257ndash265 httpdxdoiorg103354meps07175

Ruzzante de taggart ct cook d 1996 Spatial and temporal variation in the genetic composition of a larval cod (Gadus morhua) aggregation cohort contribution and genetic stability can J Fish aquat Sci 532695ndash2705 httpdxdoiorg101139cjfas-53-12-2695

Saavedra c pena Jb 2005 nucleotide diversity and pleistocene population expansion in atlantic and Mediterranean scallops (Pecten maximus and P jacobaeus) as revealed by the mitochondrial 16S ribosomal Rna gene J exp Mar biol ecol 323138ndash150 httpdxdoiorg101016jjembe200503006

Sargsyan o wakeley J 2008 a coalescent process with simultaneous multiple mergers for approximating the gene genealogies of many marine organisms Theor pop biol 74104ndash114 pMid18554676 httpdxdoiorg101016jtpb200804009

Schweinsberg J durrett R 2005 Random partitions approximating the coalescence of lineages during a selective sweep ann appl probab 151591ndash1651 httpdxdoiorg101214105051605000000430


Selkoe ka gaines Sd caselle Je warner RR 2006 current shifts and kin aggregation explain genetic patchiness in fish recruits ecology 873082ndash3094 httpdxdoiorg1018900012-9658(2006)87[3082cSakae]20co2

Shaklee Jb bentzen p 1998 genetic identification of stocks of marine fish and shellfish bull Mar Sci 62589ndash621

Siegel da kinlan bp gaylord b gaines Sd 2003 lagrangian descriptions of marine larval dispersion Mar ecol progr Ser 26083ndash96 httpdxdoiorg103354meps260083

Smith pJ benson pg Stanger c chisnall bl Jellyman bJ 2001 genetic structure of new Zealand eels Anguilla dieffenbachii and A australis with allozyme markers ecol Freshwat Fish 10132ndash137 httpdxdoiorg101034j1600-06332001100302x

So n Maes ge volckaert FaM 2006 intra-annual genetic variation in the downstream larval drift of sutchi catfish (Pangasianodon hypophthalmus) in the Mekong river biol J lin Soc 89719ndash728 httpdxdoiorg101111j1095-8312200600707x

tajima F 1989a Statistical method for testing the neutral mutation hypothesis by dna polymorphism genetics 123585ndash595 pMid2513255 pMcid1203831

tajima F 1989b The effect of change in population size on dna polymorphism genetics 123597ndash601 pMid2599369 pMcid1203832

taris n boudry p bonhomme F camara Md lapegue S 2009 Mitochondrial and nuclear dna analysis of genetic heterogeneity among recruitment cohorts of the european flat oyster Ostrea edulis biol bull 217233ndash241 pMid20040748

taylor Je 2009 The genealogical consequences of fecundity variance polymorphism genetics 182813ndash837 pMid19433628 pMcid2710161 httpdxdoiorg101534genetics109102368

taylor MS Hellberg Me 2003 genetic evidence for local retention of pelagic larvae in a caribbean reef fish Science 299107ndash109 pMid12511651 httpdxdoiorg101126science1079365

Thorson g 1950 Reproductive and larval ecology of marine bottom invertebrates biol Rev 251ndash45 httpdxdoiorg101111j1469-185X1950tb00585x

tracey Ml bellet nF gravem cd 1975 excess allozyme homozygosity and breeding population structure in mussel Mytilus californianus Mar biol 32303ndash311 httpdxdoiorg101007bF00399209

turner tF osborne MJ Moyer gR benavides Ma alo d 2006 life history and environmental variation interact to determine effective population to census size ratio proc Roy Soc b 2733065ndash3073 pMid17015350 pMcid1679889 httpdxdoiorg101098rspb20063677

turner tF Richardson lR gold JR 1999 temporal genetic variation of mitochondrial dna and the female effective population size of red drum (Sciaenops ocellatus) in the northern gulf of Mexico Mol ecol 81223ndash1229 httpdxdoiorg101046j1365-294x199900662x

turner tF wares Jp gold JR 2002 genetic effective size is three orders of magnitude smaller than adult census size in an abundant estuarine-dependent marine fish (Sciaenops ocellatus) genetics 1621329ndash1339 pMid12454077 pMcid1462333

varela Ma Martinez-lage a gonzalez-tizon aM 2009 temporal genetic variation of microsatellite markers in the razor clam Ensis arcuatus (bivalvia pharidae) J Mar biol assoc uk 891703ndash1707 httpdxdoiorg101017S0025315409000812

veliz d duchesne p bourget e bernatchez l 2006 genetic evidence for kin aggregation in the intertidal acorn barnacle (Semibalanus balanoides) Mol ecol 154193ndash4202 pMid17054512 httpdxdoiorg101111j1365-294X200603078x

wakeley J Sargsyan o 2009 extensions of the coalescent effective population size genetics 181341ndash345 pMid19001293 pMcid2621185 httpdxdoiorg101534genetics108092460

wakeley J takahashi t 2003 gene genealogies when the sample size exceeds the effective size of the population Mol biol evol 20208ndash213 pMid12598687 httpdxdoiorg101093molbevmsg024


wang J 2004 Sibship reconstruction from genetic data with typing errors genetics 1661963ndash1979 pMid15126412 pMcid1470831 httpdxdoiorg101534genetics16641963

wang J 2009 a new method for estimating effective population sizes from a single sample of multilocus genotypes Mol ecol 182148ndash2164 pMid19389175 httpdxdoiorg101111j1365-294X200904175x

wang Jl whitlock Mc 2003 estimating effective population size and migration rates from genetic samples over space and time genetics 163429ndash446 pMid12586728 pMcid1462406

waples RS 1987 a multispecies approach to the analysis of gene flow in marine shore fishes evolution 41385ndash400 httpdxdoiorg1023072409146

waples RS 1989 a generalized-approach for estimating effective population size from temporal changes in allele frequency genetics 121379ndash391 pMid2731727 pMcid1203625

waples RS 1998 Separating the wheat from the chaff patterns of genetic differentiation in high gene flow species J Hered 89438ndash450 httpdxdoiorg101093jhered895438

waples RS 2002 evaluating the effect of stage-specific survivorship on the nen ratio Mol ecol 111029ndash1037 pMid12090236 httpdxdoiorg101046j1365-294X200201504x

waples RS 2005 genetic estimates of contemporary effective population size to what time periods do the estimates apply Mol ecol 143335ndash3352 pMid16156807 httpdxdoiorg101111j1365-294X200502673x

waples RS 2006 a bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci conserv genet 7167ndash184 httpdxdoiorg101007s10592-005-9100-y

waples RS do c 2008 ldne a program for estimating effective population size from data on linkage disequilibrium Mol ecol Resour 8753ndash756 httpdxdoiorg101111j1755-0998200702061x

waples RS do c 2010 linkage disequilibrium estimates of contemporary ne using highly variable genetic markers a largely untapped resource for applied conservation and evolution evol appl 3244ndash262 httpdxdoiorg101111j1752-4571200900104x

waples RS yakota M 2007 temporal estimates of effective population size in species with overlapping generations genetics 175219ndash233 pMid17110487 pMcid1775005 httpdxdoiorg101534genetics106065300

ward Rd 2006 The importance of identifying spatial population structure in restocking and stock enhancement programmes Fish Res 809ndash18 httpdxdoiorg101016jfishres200603009

ward Rd woodwark M Skibinski doF 1994 a comparison of genetic diversity levels in marine freshwater and anadromous fishes J Fish biol 44213ndash232 httpdxdoiorg101111j1095-86491994tb01200x

watts RJ Johnson MS black R 1990 effects of recruitment on genetic patchiness in the urchin Echinometra mathaei in western australia Mar biol 105145ndash151 httpdxdoiorg101007bF01344280

whitlock Mc Mccauley de 1999 indirect measures of gene flow and migration FSt ne 1 (4nm+1) Heredity 82117ndash125 pMid10098262 httpdxdoiorg101038sjhdy6884960

winemiller ko Rose ka 1992 patterns of life-history diversification in north american fishes implications for population regulation can J Fish aquat Sci 492196ndash2218 httpdxdoiorg101139f92-242

wright S 1931 evolution in Mendelian populations genetics 28139ndash156wright S 1938 Size of population and breeding structure in relation to evolution Science

87430ndash431yamamoto S uchida k Sato t katsura k takasawa t 2007 population genetic structure and

effective population size of ayu (Plecoglossus altivelis) an amphidromous fish J Fish biol 70191ndash201 httpdxdoiorg101111j1095-8649200701396x


Zouros e pogson gH 1994 Th e present status of the relationship between heterozygosity and heterosis In beaumont a editor genetics and evolution of aquatic organisms london chapman amp Hall p 135ndash146

date Submitted 11 June 2010date accepted 8 november 2010available online 7 december 2010

addresses (dH) Department of Biological Sciences University of Southern California Los Angeles California 90089-0371 (aip) Institute of Marine Biology Vladivostok 690041 Russia corresponding author (dH) E-mail ltdhedgeuscedugt


the hypothesis discuss its predictions and the methods for and limits to testing those predictions review evidence that has accumulated for the hypothesis and finally draw implications about the place of SRS in contemporary marine science

the Hypothesis of Sweepstakes Reproductive Success

Most marine animals have ecologically distinct adult and larval stages with high fecundity and high early mortality or type iii survivorship (Thorson 1950 winemiller and Rose 1992) larvae of such species typically develop for weeks in the plankton are microscopic weakly swimming easily dispersed by ocean currents and subject to high mortality resulting in erratic recruitment to adult populations (cushing 1990) Survival growth and behavior of these larval forms influence recruitment success population connectivity and the distribution and abundance of adult populations (cowen et al 2006 2007) which tend to occupy vast geographic ranges and often comprise tens of millions to billions of individuals in many cases based on catch statistics yet these large marine populations generally have only fractions of the genetic diversity expected from their sheer abundance (Hedgecock et al 1982 nei and graur 1984 avise et al 1988 palumbi and wilson 1990 avise 1994 grant and bowen 1998) and despite widely dispersing planktonic larvae and high genetic similarity over broad spatial scales often show chaotic genetic heterogeneity on small spatial scales (Johnson and black 1984 watts et al 1990 Hedgecock 1994b edmands et al 1996 david et al 1997 recent literature reviewed by Hauser and carvalho 2008) to explain both of these paradoxical observations one of us (dH) hypothesized that marine animals in general have extremely large variance in individual reproductive success owing to sweepstakes-like chances of matching reproductive activity with oceanographic conditions conducive to gamete maturation fertilization larval development settlement and recruitment to the adult spawning population (Hedgecock et al 1982 p 322ndash324 Hedgecock 1982 Hedgecock 1994a)

the population genetic effect of SRS is captured by wrightrsquos (1938) equation Ne asymp (4N minus 2) ∕(Vk + 2) in which Ne is the effective population size N is the size of the breeding population and Vk is the variance in number of offspring (k) con-tributed per parent to the adult spawning population in the Fisher-wright model of a diploid population with non-overlapping generations and constant size kr = 2 Vk asymp 2 (ie the variance of a poisson or binomial distribution of offspring number) and Ne asymp N in real populations Vk may exceed that of the ideal population reducing Ne relative to N (see crow and denniston 1988) The SRS hypothesis says that Vk is often large enough in highly fecund marine animal populationsmdash102 and potentially much highermdashto reduce the ratio of effective to actual population numbers NeN asymp 4 (Vk + 2) to a small fraction (ltlt 001) Though somewhat arbitrary this quantitative defini-tion of SRS contrasts sharply both with the theoretical conclusion that the NeN ratio should rarely be below 05 (nunney 1996) and also with a meta-analysis reporting an average NeN ratio of 011 across 192 studies mostly of terrestrial species taking fluctuating population size unequal sex ratio and variance in reproductive success into account (Frankham 1995) Though Vk is certainly enhanced in marine species by widespread failure to reproduce Hedrick (2005) shows that a few very successful breeders can make the NeN ratio small even if a sizeable fraction of the population




















citation analyses
















temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited




















































































































































































































citation analyses
















temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited














































































































































































































citation analyses
















temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited









































































































































































































citation analyses
















temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited




































































































































































































citation analyses
















temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited














































































































































































































temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited









































































































































































































temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited






































































































































































































temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited


































































































































































































temporal Studies







cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited




































































































































































































cohort Studies





































discussion
























1) and new recruits











acknowledgments


literature cited



































































































































































































































discussion
























1) and new recruits











acknowledgments


literature cited





























































































































































































































discussion
























1) and new recruits











acknowledgments


literature cited
























































































































































































































discussion
























1) and new recruits











acknowledgments


literature cited


















































































































































































































discussion
























1) and new recruits











acknowledgments


literature cited














































































































































































































discussion
























1) and new recruits











acknowledgments


literature cited



































































































































































































discussion
























1) and new recruits











acknowledgments


literature cited




















































































































































































































1) and new recruits











acknowledgments


literature cited















































































































































































































1) and new recruits











acknowledgments


literature cited











































































































































































































1) and new recruits











acknowledgments


literature cited









































































































































































































acknowledgments


literature cited




































































































































































































acknowledgments


literature cited




































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































Documents

SWEEP STAKE S REPR ODUCTIVE SUCCE SS IN HIG … · HEDGECOCK AND PUDOVKIN : SWEEPSTAKES REPRODUCTIVE SUCESS 973 leaves an average of two o spring for replacement; further, with SRS,