ICES CM 2009 /H:06

Not to be cited without prior reference to the author

The evolution of alternative migratory tactics: lessons from anadromous

salmonids

Julian Dodson1, Nadia Aubin-Horth2, Véronique Thériault3 and David Paez1

1Département de biologie, Pavillon Vachon, 1045, avenue de la Médecine, Université Laval, Québec (Québec) G1V 0A6, Canada 2Institut de Biologie Intégrative et des Systèmes (IBIS), Pavillon Charles-Eugène-Marchand, 1030, avenue de la Médecine, Université Laval, Québec (Québec) G1V 0A6 Canada 3Hatfield Marine Science Center, Marine Fisheries Genetics Program, Oregon State University, 2030 SE Marine Science Drive, Newport, OR 97365, USA

Abstract: Alternative life-history tactics are common in fishes and many cases involve

resident and migratory life styles. The resident tactic may involve both sexes or be

restricted to males. Disruptive selection favouring alternative tactics may arise from two

different evolutionary mechanisms. On the one hand, alternative migratory tactics may be

the result of sexual selection for alternative reproductive phenotypes that impact other

aspects of life-history, including resource exploitation. On the other hand, alternative

migratory tactics may be caused by natural selection favouring divergence to exploit

multiple niches which in turn impacts reproductive tactics. Frequency dependent

selection plays a central role in maintaining alternative reproductive tactics and their

1

ICES CM 2009 /H:06

associated migratory phenotypes in natural populations. However, in cases where

individuals exploit multiple niches, natural selection favours multiple specialized

phenotypes and frequency dependent selection is not necessarily expected to be

important. Based on anadromous salmonids, we summarize evidence that (1) alternative

migratory tactics co-exist within single gene pools and that individuals may potentially

adopt one or the other alternative phenotype. The expression of different migratory

phenotypes is a function of sex and condition (growth or some correlated trait) and is

under both environmental and genetic control. Non-linear reaction norms that underlie

alternative life-history phenotypes vary among species and among different ages of the

same species. (2) The suppression of frequency-dependent selection may underlie the

existence of two common gradients observed anadromous salmonids: increasing

residency with altitude or distance upstream, and increasing anadromy at higher latitudes.

Anadromy may also be subjected to the forces driving the evolution of dispersal within

metapopulations, with selection favouring increased dispersal in more northerly

populations characterised by greater environmental stochasticity. The interplay between

condition-dependant alternative migratory tactics and condition-dependent dispersal in

metapopulations determines the degree of population genetic structure through its

influence on reproductive isolation and gene flow.

Introduction

A variety of migratory patterns co-exist within populations of most salmonid fishes.

Individual fish comprising a population may complete their entire lifecycle in freshwater

streams (residency) whereas others may migrate to sea (anadromy) or to lakes (e.g.

Olsson and Greenburg 2004) before returning to freshwater streams to spawn. Originally

referred to as partial migration (Jonnson and Jonnson 1993), these different migratory

tactics are generally associated with important differences in body sizes in adult

reproductive fish. As variation in body size has an important impact on reproductive

2

ICES CM 2009 /H:06

success, both sexual and natural selection must be considered to understand the evolution

of alternative migratory tactics (AMTs).

Size polymorphisms may be the result of sexual selection for alternative reproductive

tactics (ARTs) (Brockman and Taborsky 2008). Intense intra-sexual selection is a

characteristic of such mating systems and involves high variance in reproductive success

among individuals of the same sex (Schuster and Wade 2003). Sexual selection can be

important in producing the ART most commonly observed in fishes. Under a 1:1 sex

ratio, if some males monopolize and mate with several females, other males will

necessarily fail to reproduce. This intra-sexual competition strongly favours alternative

mating phenotypes (Shuster and Wade 2003). In salmonids, these are generally

represented by bourgeois males that monopolize mates using their large body size and

secondary sexual characteristics, and small parasitic males that exploit bourgeois males

by sneaking fertilisations (Taborsky 2008). It is more difficult to identify ARTs related to

intense intra-sexual competition among females. The female equivalent of male

parasitism would be intraspecific brood parasitism (placing eggs in another females nest,

for example). However, given the predominance of external fertilisation in fishes, brood

parasitism is expected to be rare (Taborsky 2008). Cooperative breeding is another

example; smaller, subordinate mature females may participate in reproduction. But given

the almost complete absence of parental care in salmonid fishes, there seems to be little

opportunity for cooperative breeding. A third possibility is that disruptive selection on

body size in females is a result of female competition for oviposition sites (Fleming and

Gross 1994).

In other cases, non-sexual selection on non-reproductive traits may provide the conditions

required for the evolution of AMTs and lead to the evolution of ARTs as a consequence.

Any morphological or metabolic variation that improves foraging success in one habitat

may lead to the development of alternative foraging tactics. If such tactics lead to

important size differences, the stage is set for the development of ARTs. In such cases,

non-sexual selection favours size dimorphism.

3

ICES CM 2009 /H:06

We must thus consider the simultaneous action of two evolutionary mechanisms to

understand the development and maintenance of AMTs. They are influenced to some

extent by sexual selection for alternative reproductive tactics that impact other aspects of

life-history, particularly foraging tactics that directly influence metabolism and growth.

Simultaneously, alternative migratory tactics are influenced by non-sexual selection

favouring ecological divergence across multiple niches which in turn impacts

reproductive tactics. The two sources of selection are inseparable in any discussion of

alternative migratory tactics.

Our purpose in this presentation is to review the evidence that alternative migratory

tactics are maintained under a threshold-trait model (Roff 1996). We first consider the

evidence that alternative migratory tactics co-exist within a single gene pool and that

individuals may potentially adopt one or the other alternative phenotype. We then look at

the evidence that the expression of different migratory phenotypes is a function of some

environmental cue. We also consider the evidence that a genetic component plays a role

in the development of the alternative migratory phenotypes. Second, we explore the

basis of alternative migratory and reproductive tactics among female salmonids whose

mating success may be relatively free of frequency-dependant selection. Thirdly, we aim

to apply this knowledge to understanding the biogeography of AMTs, in particular the

observation that residency tends to increase within rivers upstream and at higher altitudes

and that anadromy is favoured at higher latitudes.

I - The importance of condition-dependant selection in the maintenance of alternative

migratory tactics.

For an alternative phenotype to invade a population and to persist, the average fitness of

the alternative phenotype when it is rare must be greater than the average fitness of the

conventional phenotype and, to persist in a population at a stable frequency, the average

fitness of the alternative phenotype at equilibrium must equal the average fitness of the

conventional phenotype (Schuster and Wade 2003). Together, these conditions define

4

ICES CM 2009 /H:06

negative frequency-dependant selection which is associated with crossing fitness curves

of alternative phenotypes (Brockman and Taborsky 2008, Fig. 1).

Figure 1. Negative frequency dependant selection acting on hypothetical migrant and resident male phenotypes. Migrants with large body sizes adopt a bourgeois mating tactic whereas small-bodied residents adopt a sneaker mating tactic. The success of each morph depends on its frequency in the population, each doing better when rare. The relative frequency of each phenotype stabilizes at a point where the average fitness of each phenotype is equal (the evolutionary stable state, ESS). (modified from Brockman and Taborsky 2008).

Developmental and behavioural strategies, which are commonly associated with

salmonid alternative mating strategies (Gross 1985, Hutchings and Myers 1994) result

from the interaction between the environment and an individual’s genome, coupled with

a genetically determined threshold of sensitivity. Such developmental trajectories may be

considered as threshold traits whose expression is controlled by many loci of small

effects rather than in a Mendelian fashion (Roff 1996). Each genotype possesses its own

threshold and the expressed phenotype is a function of the genotype and the environment.

Individuals with phenotypes that exceed the threshold tend to display one reproductive

tactic, while individuals with phenotypes falling below the threshold display the

alternative reproductive tactic (Hutchings and Myers 1994, Figure 2).

5

ICES CM 2009 /H:06

Figure 2. Threshold traits and discrete developmental phenotypes. (A) Threshold reaction norms are non-linear functions defining the probability of different genotypes to express a dimorphic trait (eg. migrate, stay) as a function of a switch point and environmental variation. For a given genotype, individuals with phenotypes below the switchpoint express a default tactic (X); phenotypes above the threshold express a modified tactic (Y). (B) There is a normal distribution of switchpoints (F(sp)) in the population. At any specific value of the environmental clue, the environmentally determined threshold (e*) defines the relative frequency of the two tactics in the population. (modified from Tomkins and Hazel 2007).

The condition dependent selection hypothesis suggests that the environment will select

for a mean threshold value and that this value may thus vary among populations facing

different environments. Using common garden experiments, Piché et al. (2008)

demonstrated genetic differentiation among populations of Atlantic salmon for thresholds

of precocious maturity.

When the fitness consequences of alternative behavioural phenotypes depend on the

relative competitive ability of interacting individuals (i.e. their relative status), then

6

ICES CM 2009 /H:06

selection is said to be status dependent (Gross 1996). Status may be considered as a

threshold trait and the status-dependent selection model may thus be considered as being

equivalent to the condition-dependant model if individuals have genetic variation for

switchpoints and populations have different mean threshold values (Tomkins and Hazel

2007).

Figure 3. Status-dependant selection. (A) The distribution of condition (status) in the population and the fitness (F) functions of the resident and migrant phenotype in a population. Fitness functions cross over and are thus frequency dependent. The intersection of the two fitness functions defines the evolutionary stable switch point where the fitness of each phenotype is equal. Low status fish maximize their fitness by developing as migratory fish that delay reproduction and adopt the bourgeois behavioural repertoire while high status fish maximize their fitness by suspending migration, maturing early and adopting the sneaker behavioural repertoire. (B) If the average fitness of the resident phenotype declines due to density-dependent competition for example (eg. Fleming and Gross 1994), the switch point shifts towards higher status thus reducing the frequency of residents in the population and re-establishing the evolutionary stable state (modified from Tomkins and Hazel 2007).

In salmonids, many different patterns of alternative migratory strategies exist. In

predominantly anadromous populations of Atlantic salmon (Salmo salar) for example, all

females are anadromous and only the males exhibit the residency/anadromy dichotomy

(Hutchings and Myers 1994). In Pacific salmonids (Oncorhynchus sp.), both sexes are

anadromous, but some anadromous males may spend only several months at sea before

7

ICES CM 2009 /H:06

returning to freshwater to spawn (jacks) relative to others that may stay at sea for several

years (eg Gross 1991). Strictly freshwater resident males occur but are rare (residual

sockeye salmon, for example (Ricker 1938)). In other species of salmonids, both males

and females may exhibit the residency/migratory dichotomy, exploiting streams, rivers,

estuaries and the open ocean for feeding (eg. brook charr Salvelinus fontinalis, Theriault

and Dodson 2003, Lenormand et al. 2003; arctic charr Salvelinus alpinus, Nordeng 1983;

rainbow trout Oncorhynchus mykiss, Pascual et al. 2001; brown trout Salmo trutta;

Jonsson, 1985) such that both sexes may exhibit considerable variance in body size at the

moment of reproduction.

Does the hypothesis of condition-dependant selection apply to alternative migratory

phenotypes? Firstly, we must establish that alternative migratory tactics co-exist within a

single gene pool and that individuals may potentially adopt one or the other phenotype.

Much empirical evidence exists to support the proposition that the sympatric occurrence

of alternative migratory phenotypes in salmonids is not accompanied by genetic

differentiation when the alternative phenotypes occupy the same spawning grounds at the

same time (Arctic charr (anadromous, small and large freshwater residents) (Nordeng

1989), anadromous and freshwater brown trout (Hinder et al. 1991, Charles et al. 2005,

Charles et al. 2006), anadromous steelhead and resident O. mykiss (Docker & Heath

2003, Olsen et al. 2006, McPhee et al. 2007), resident and anadromous brook charr

(Thériault et al (2007)). They may therefore be considered as conditional tactics

expressed within common gene pools. In cases where residency is restricted to males, as

in predominantly anadromous populations of Atlantic salmon, no such differentiation can

occur as early maturing parr must necessarily spawn with anadromous females.

Second, we must establish if the expression of different migratory phenotypes is a

function of some environmental cue. Assuming that individual growth performance

integrates environmental variation and is the most reliable indicator of condition, we may

then ask if the expression of different migratory phenotypes is related to growth (or body

size-energy reserves). Several studies have supported the hypothesis that faster growing

individuals migrate to more productive feeding areas than slower-growing individuals

8

ICES CM 2009 /H:06

because they maintain higher metabolic rates and are energetically constrained at a

younger age (or smaller size) than slow-growers (brown trout, Forseth et al. 1999, brook

charr, Morinville and Rasmussen 2003). Thus fast growth leads to migration and the

exploitation of richer feeding grounds. However, other studies have shown that fast early

growth is associated with freshwater residency and, in some cases, early male maturity

(brown trout Olsson et al. (2006), Atlantic salmon (Rowe and Thorpe 1990, Aubin-Horth

and Dodson 2004).

Third, we must also establish that genetic variation for the threshold level exists among

individuals. Several studies have shown a significant heritable component in the

development of alternative migratory tactics (eg. chinook salmon (Oncorhynchus

tshawytscha) Heath et al. 2002, Atlantic salmon, Garant et al. 2003, brook charr,

Thériault et al. 2007). However, this does not necessarily mean that the male offspring of

one phenotype will be composed mainly of that phenotype because of the role of

environmental variation. For example, resident Atlantic salmon fathers may produce

more anadromous offspring if the offspring experience poor growth conditions. These

anadromous fish in turn will father resident male offspring if growth conditions improve.

Complicating further this relationship, growth shows high heritability in salmonids

(Garcia De Leaniz et al. 2007). It is plausible then that the relationship found between the

tactic of the father and that of the sons in a given environment could be explained largely

by the heritability of growth rate or size, rather than the heritability of the threshold size,

leading to the expression of the same tactic as the father. Some support for this

hypothesis was provided by Garant et al. (2002) who found that young Atlantic salmon

fathered by precocious males grew faster than those fathered by anadromous males

during the time from hatching to yolk sac absorption. In contrast, Morrasse et al. (2008)

working with the same Atlantic salmon population as Garant et al. (2002) demonstrated

in the laboratory that weight, length, and protein content of the progeny of anadromous

and sneaker males did not differ.

Experiments were conducted to determine if the higher incidence of Atlantic salmon

sneaker males in the upstream sites of the Ste-Marquerite R. documented by Aubin-Horth

et al. 2006, is due to selection acting on growth thresholds, or whether it is due to varying

9

ICES CM 2009 /H:06

growth opportunities particular to the different sites. Wild anadromous and sneaker

progenitors from upstream and downstream sites were used in a factorial mating design.

Families were reared in captivity, and individual growth of PIT-tagged age-1 fish was

monitored for an additional 10 months, at which time all male progeny were either smolts

or sexually mature. No difference in the incidence of smolt and sneaker male progeny

was observed between upstream and downstream sites or between the two paternal

reproductive tactics. However, 42% of the total variation was explained by the variation

in incidence among sire groups, providing preliminary evidence of genetic variation in

the incidence of alternative migratory and reproductive tactics. Second, the predicted

growth asymptote differed between offspring that matured as sneakers and offspring that

smolted, with smolt attaining larger body sizes than mature parr as previously

documented (Fig. 4).

Figure 4. Differences in asymptotic length for smolt (left) and sneaker parr (right) offspring originating from different paternal tactics (F-fighter, S-sneaker) in upstream (U) and downstream (D) sites. Significant differences were seen only in the smolts (stars). Error bars are 95% CI. Please note different y-axis scales.

Third, even though no effects from the paternal tactic and its population of origin were

observed for sneaker parr, significant growth variation among mature parr offspring

between sire groups was observed (LRT = 227.3, P-value < 0.001) (Fig. 5). Because

10

ICES CM 2009 /H:06

common environmental effects, repeated measurements made on each individual and

maternal effects are accounted for, the variation among sire groups is evidence of genetic

variation for growth rates.

Figure 5. Fig. 5. Variation in asymptotic size among mature parr offspring of fighter (F) and sneaker (S) sires. Error bars are 95% confidence intervals

Evidence exist that population reaction norms associating growth or size with migratory

strategies are highly plastic, varying as a function of age, sex and possibly parental tactic.

In brook charr, migration first occurs at the age of 1+ and outmigrants are among the

bigger, most metabolically active juvenile fish. However, outmigration also occurs at the

age of 2+ and outmigrants are among the smallest juvenile fish. The largest juveniles

remain in freshwater and begin spawning the following year (Thériault and Dodson 2003,

Thériault et al. 2008). Furthermore, the sex ratio of outmigrants is male-biased among 1+

fish and female biased among 2+ fish, suggesting somewhat different selective pressures

on male and female migration thresholds. Rikardsen et al. (1997) also found that more

male than female Arctic charr migrated at a younger age. Ricker (1938) formulated a 2-

step scenario while studying anadromous and residual (freshwater resident phenotype)

sockeye salmon in Canada. Fast-growers matured in freshwater, medium growers

migrated at 1+ and slow growers decided upon migration or residency the following year.

Among these, the fastest growing fish remained resident and matured in fresh water

whereas the slowest-growing fish migrated at 2+.

11

ICES CM 2009 /H:06

The frequency dependent nature of alternative reproductive tactics in males suggests that

alternative migratory tactics must also be influenced by frequency dependent selection

acting during breeding. However, there is little empirical evidence either for or against

this hypothesis. We may speculate that a reduction in the proportion of migratory fish,

particularly among males, will cause an increase in the proportion of resident males. As

resident fish experience less mortality than do migrants (eg brook charr, Thériault et al.

2008) we would expect the overall density of males on the spawning grounds to also

increase, thus altering the operational sex ratio and the number of males competing for

females at any point in time. Experiments that artificially manipulate overall density and

the relative proportions of resident and migratory phenotypes are needed to evaluate how

the mating success of different migratory phenotypes changes as a consequence. We

would expect that foraging decisions and associated migratory tactics may be modulated

and constrained by differential mating success on the spawning grounds.

In conclusion, the hypothesis of condition-dependant selection applies reasonably well to

alternative migratory tactics in salmonids. Most, but not all, cases of AMTs co-exist

within common gene pools. Secondly, the expression of alternative phenotypes appears

to be a function of individual condition (expressed as growth rate, body size or some

correlated measure). In some cases, faster growing individuals choose to migrate to more

productive habitats whereas in other cases, slower growers migrate. Genetic

differentiation among populations for thresholds of precocious maturity has been

demonstrated supporting the threshold-trait, condition dependant model. The significant

variation in the nature of the reaction norms associating growth (or some surrogate

measure of condition) and migratory/reproductive phenotype observed among paternal

types, populations and species suggests that phenotypic plasticity plays a predominant

role in the origin and maintenance of AMTs.

II - Alternative female migratory strategies

12

ICES CM 2009 /H:06

Given the absence of brood parasitism and cooperative breeding in most female

salmonids, disruptive selection acting upon females to produce different migratory

phenotypes may be associated with competition for breeding sites. There is strong

competition among females for the best spawning sites and body size is a major factor in

determining the winner of such contests (van den Berghe and Gross 1989, Fleming and

Gross 1994). There is evidence that females of different sizes exploit streams and

spawning grounds of different dimensions (Fig.5) such that the maintenance of different

body sizes among females may reduce competition among females for oviposition sites.

Smaller females should do better in smaller streams with smaller substrate sizes and more

spatially restrained spawning sites than bigger females. Such an advantage may

counterbalance the loss of fecundity associated with smaller size. Under such a scenario,

alternative female phenotypes will not be under frequency-dependant selection as the

mating success of one phenotype will not detract from the mating success of the

alternative. Rather, their relative abundance will depend upon the relative abundance of

the spawning habitats and not on the frequency of the alternative phenotype. Large

anadromous males can displace small males in a variety of salmonids species, (eg.

anadromous coho salmon, Fleming and Gross 1994). We speculate that in spatially

constrained spawning habitats, small males may be restricted to breeding with small

females. In such spatially constrained habitat, both males and females could be released

from frequency-dependent selection favouring the loss of the anadromous phenotype

from both sexes. This may lead to the development of isolated populations of small fish

inhabiting small streams within the drainage basin. This could happen in the absence of

geographical isolation and may represent a case of isolation through adaptation (Nosil

and Funk 2008) rather than isolation by distance or physical barrier.

13

ICES CM 2009 /H:06

Figure 5. The size distribution of anadromous male and female brook charr in the main stem and anadromous and resident brook charr in a tributary stream of the St. Marguerite River, Québec Canada. Anadromous fish found in the spawning tributary stream are the smallest of the anadromous fish, both sexes combined.

III - The biogeography of alternative migratory tactics

Two major gradients in the incidence of alternative migratory strategies have been

documented in salmonids fishes: increasing residency with altitude or distance upstream,

and increasing anadromy at higher latitudes. A number of studies have demonstrated that

the incidence of anadromy in partially migratory salmonid populations tends to diminish

with altitude and/or distance upstream and that anadromous individuals preferentially

occupy the lower reaches of their nursery rivers. In two separate studies, male parr of

Atlantic salmon of a given age and size were more likely to be sexually mature if located

further upstream/at higher altitudes (Baum et al. 2004, Aubin-Horth et al. 2006). Both

studies concluded that the gradient reflected the increasing costs of migration. In brown

trout, the recruitment of anadromous populations declined with altitude relative to that of

resident populations illustrating a cost of migration positively correlated with altitude

(Bohlin et al. 2001). Several studies have demonstrated that resident fish are found

14

ICES CM 2009 /H:06

further upstream than anadromous fish of the same population (brook charr (Curry 2005),

Dolly Varden (Salvelinus malma) (Armstrong and Morrow 1980), rainbow trout (Riva-

Rossi et al. 2007)).

These observations are consistent with the hypothesis that increased migratory costs

favour residency over anadromy as distances to spawning grounds increase. Migratory

costs may include significant energy expenditures during the upstream migration

(Dodson 1997, Jonsson and Jonsson 2006) as well as an increasing probability of losing

access to upstream or higher elevation spawning grounds because of low discharge and/or

high summer temperatures (Aubin-Horth et al. 2006). If the average fitness of the

migrant male phenotype declines due to mortality selection (Endler 1986) or an increased

probability of exclusion from the spawning grounds, the reproductive success of residents

may exceed that of migrants independent of variations in condition (body size or growth).

If the fitness curves of the two tactics no longer intersect (Fig. 4), negative frequency

dependent selection would no longer play a significant role in determining the incidence

of alternative reproductive tactics among males and the resident tactic would be favoured.

In the case of females, fecundity selection and competition among females favours body

size (Fleming and Gross 1994) such that the anadromous tactic should always garner the

greatest fitness benefits. A resident phenotype would only be expected to develop in

females in cases of extreme mortality selection against the anadromous phenotype. The

many cases that document the development of land-locked populations above impassable

barriers to migration, whether they are natural (e.g. rainbow trout, Kostow 2003) or

artificial (eg. white-spotted charr, Yamamoto et al. 2004), represents an extreme situation

whereby downstream migrants cannot return to spawning sites and the migratory

phenotype is culled from both males and females.

Considerable evidence exists to demonstrate that anadromous phenotypes of many

salmonid species predominate at higher latitudes (Dolly Varden (Maekawa and Nakano

2002), white-spotted charr (Salvelinus leucomaenis), (Yamamoto et al 1999), cherry trout

(Oncorhynchus masou) (Kato 1991), brook charr (Castric et al. 2003), rainbow trout

(McPhee et al. 2007)). The latitudinal gradient in anadromy is to some extent the result of

15

ICES CM 2009 /H:06

the altitudinal gradient previously mentioned. As downstream areas at the southerly limits

of distribution are less and less hospitable for juvenile rearing because of temperature

constraints (among other habitat variables), anadromous fish must migrate greater

distances upstream and to higher latitudes to insure that their young are associated with

appropriate rearing habitat. Thus, the cost of migration increases and the average

reproductive success of anadromous phenotypes declines to the point where fitness

curves may no longer intercept. In such a case, frequency dependent selection no longer

plays a role and natural selection culls the anadromous strategy from the most southerly

populations.

This mechanism however does not explain why the frequency of the resident phenotype

should decline at higher latitudes. Several mechanisms may be involved. The food

availability hypothesis proposes that anadromy evolves in situations where marine

productivity is greater than productivity in freshwater (Gross et al. 1988). The importance

of food intake for body growth and the contribution of growth to fitness through

increased fecundity and improved male and female breeding success have been

documented (Gross et al. 1988). This hypothesis was originally formulated to explain the

difference in the latitudinal distribution of anadromy and catadromy. It was based on a

species level analysis ranging from 0 to 75 degrees of latitude. The original food

availability hypothesis has been subsequently appropriated by many authors to explain

intraspecific differences in the incidence of anadromy of salmonids exhibiting alternative

migratory tactics across rather limited latitudinal ranges. This particular interpretation of

the original hypothesis is incorrect for several reasons. Estuaries and adjacent coastal

waters are among the most productive habitats on the planet and growth in such habitats

will always be better relative to that achieved in upstream fresh waters. If anadromy is

uniquely the result of selection for increased body size, migration to estuarine habitat in

salmonids would always be favoured. Secondly, body size is not simply the result of

ecosystem productivity. Size at age is also influenced extrinsically by the length of

growing season and intrinsically by the balance between rates of anabolism and

catabolism that determines growth rate. Some studies have demonstrated that fish from

high-latitudes have a higher capacity for growth than their low-latitude conspecifics at the

16

ICES CM 2009 /H:06

same temperature (Conover and Present 1990). As such, the reaction norms of growth as

a function of temperature are greater at high latitudes. This may involve two types of

trade-offs (Angilletta et al. 2003); allocation trade-offs between different functions and

acquisition trade-offs, whereby an increase in foraging results in an increase in mortality.

If higher mortality is a result of increased foraging at high latitudes (eg. Langford et al.

2001), switching to more productive habitats could increase the average fitness of the

anadromous phenotypes relative to the resident phenotype at high latitudes. As such, the

benefits of foraging in more productive marine environments is realised only when

foraging in freshwater involves acquisition trade-offs.

One benefit of the migratory phenotype not yet considered is that migration provides the

opportunity to disperse and reproduce elsewhere. Alternative migratory phenotypes are

thus also subjected to the forces driving the evolution of dispersal (Castric and

Bernatchez 2003). In the context of metapopulation theory, factors acting at the between-

population level favour dispersal. In particular, variation in population size caused by

habitat disturbance, ecological succession and demographic stochasticity may all favour

dispersal, while a costly dispersal form should decline in frequency in more stable

habitats and populations (Olivieri et al. 1995). Recent theoretical work has shown

selection for increased dispersal in metapopulations with high environmental

stochasticity and low dispersal costs (Bonte and de la Pena 2009). Along the eastern coast

of North America, anadromous salmonids have dispersed northwards from southern

refugia over the past 15 000 years since the last glacial maximum. Populations at

northern latitudes have thus been more recently founded than those found further south

(eg. brook charr, Castric and Bernatchez 2003). If environmental stochasticity increases

with latitude, we may expect greater levels of dispersal and hence a greater incidence of

the migratory tactic in the more recently founded and more environmentally stochastic

populations found at higher latitudes. At present, the interface between condition-

dependant alternative migratory tactics and condition-dependent dispersal in

metapopulations has yet to be explored.

17

ICES CM 2009 /H:06

References Angilletta M.J., Wilson R.S., Navas C.A., James R.S. 2003. Trade offs and the evolution

of thermal reaction norms. Trends in Ecology and Evolution 18: 234-240.

Armstrong, R.H., Morrow, J.E. 1980. The Dolly Varden. In: Balon, E.K., ed. Charrs:

Salmonid fishes of the genus Salvelinus. The Hague: Dr. W. Junk Publishers. Pp.

99-140.

Aubin-Horth, N., Dodson, J.J. 2004. Influence of individual body size and variable

thresholds on the incidence of a sneaker male reproductive tactic in Atlantic

salmon. Evolution 58: 136-144.

Aubin-Horth, N., Bourque, J-F., Daigle, G., Hedger, R.D., Ddodson, J.J. 2006.

Longitudinal gradients in threshold sizes for alternative male life history tactics in

a population of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and

Aquatic Sciences. 63 : 2067-2075.

Baum D., Laughton R., Armstrong J., Metcalfe N. 2004. Altitudinal relationship between

growth and maturation rate in salmon parr. Journal of Animal Ecology 73: 253-

260.

van den Berghe E.P., Gross M.R. 1989. Female size and nest depth in coho salmon

(Oncorhynchus kisutch). Canadian Journal of Fisheries and Aquatic Sciences 41:

204-206.

Bohlin T., Pettersson J., Degerman E. 2001. Population density og migratory and resident

brown trout (Salmo trutta) in relation to altitude: evidence for migration coast.

Journal of Animal Ecology 70:112-121

Bonte D., de la Pena E. 2009. Evolution of body-condition dependent dispersal in

metapopulations. Journal of Evolutionary Biology 22: 1242-1251.

Brockman H.J., Taborsky M. 2008. Alternative reproductive tactics and the evolution of

alternative allocation phenotypes. In Oliveira, R.F., Taborsky M., Brockman H.J.

eds. Alternative Reproductive tactics: an integrative approach. Cambridge

University Press. Pp 25-51.

Castric V., and Bernatchez, L. 2003. The rise and fall of isolation by distance in the

anadromous brook charr (Salvelinus fontinalis Mitchill). Genetics 163: 983-996.

Charles, K., Guyomard, R., Hoyheim, B., Ombredane, D., Baglinière, J.-L. 2005. Lack of

18

ICES CM 2009 /H:06

genetic differentiation between anadromous and non-anadromous sympatric trout

in a Normandy population. Aquatic Living Resources 18: 65–69.

Charles K, Roussel J-M, Lebel J-M, Baglinière J-L. 2006. Genetic differentiation

between anadromous and freshwater resident brown trout (Salmo trutta L.):

insights obtained from stable isotope analysis. Ecology of Freshwater Fish. 15:

255–263.

David O. Conover D.O., Present T.M.C., 1990. Countergradient variation in growth rate:

compensation for length of the growing season among Atlantic silversides from

different latitudes. Oecologia 83: 316-324.

Curry R.A. 2005. Assessing the reproductive contributions of sympatric anadromous and

freshwater-resident brook trout. Journal of Fish Biology 66: 741–757

Docker M.F., Heath D.D. 2003. Genetic comparison between sympatric anadromous

steelhead and freshwater resident rainbow trout in British Columbia, Canada.

Conservation Genetics 4: 227-231.

Dodson, J.J. 1997. Fish Migration: an evolutionary perspective. In Godin, J.-G. ed.

Behavioral Ecology of Teleost Fishes. Oxford University Press. pp. 10-36.

Endler J.A. 1986. Natural selection in the wild. Princeton University Press, Princeton,

N.J.

Fleming I., Gross M.R. 1994. Breeding competition in a Pacific salmon (Coho:

Oncorhynchus kisutch): measures of natural and sexual selection. Evolution 48:

637-657.

Forseth T., Næsje T.F., Jonsson B., Harsaker K. 1999. Juvenile migration in brown trout:

a consequence of energetic state. Journal of Animal Ecology 68: 783-793.

Garcia de Leaniz C., Fleming I. A., Einum S. et al. 2007. A critical review of adaptive

genetic variation in Atlantic salmon: implications for conservation. Biological

Reviews 82: 173–211.

Garant, D., Fontaine, P.-M., Good, S.P., Dodson, J.J., Bernatchez, L. (2002). Influence of

male parental identity on growth and survival of offspring in Atlantic salmon

(Salmo salar). Evolutionary Ecology Research 4: 537-549.

Garant, D., Dodson, J.J., Bernatchez, L. 2003. Differential reproductive success and

heritability of alternative reproductive tactics in wild Atlantic salmon. Evolution

19

ICES CM 2009 /H:06

57: 1133-1141.

Gross M.R. 1985. Disruptive selection for alternative life histories in salmon. Nature 313:

47-48.

Gross, M. R., R. M. Coleman and R. M. McDowall. 1988. Aquatic productivity and the

evolution of diadromous fish migration. Science 239:1291-1293.

Gross M.R. 1991. Evolution of alternative reproductive strategies: frequency-dependent

sexual selection in male bluegill sunfish. Philosophical Transactions of the Royal

Society London B 332: 59-66

Heath D.D., Rankin L., Bryden C.A., Heath J.W., Shrimpton J.M. 2002. Heritability and

Y-chromosome influence in the jack male life history of chinook salmon

(Oncorhynchus tshawytscha) Heredity 89: 311-317

Hindar K., Jonsson B., Ryman N., Stahl G. 1991. Genetic relationships among

landlocked, resident, and anadromous brown trout, Salmo trutta L. Heredity 66:

83-91.

Hutchings, J.A., Myers R.A. 1994. The evolution of alternative mating strategies in

variable environments. Evolutionary Ecology 8: 256-268.

Jonsson, B. 1985. Life history patterns of freshwater resident and sea-run migrant brown

trout in Norway. Transactions of the American Fisheries Society 114: 182–194.

Jonsson B., Jonsson N. 2006. Life history effects of migratory costs in anadromous

brown trout. Journal of Fish Biology 69: 860-869.

Jonsson, B., Jonsson, N. 1993. Partial migration: niche shift versus sexual maturation

in fishes. Reviews in Fish Biology and Fisheries 3: 348–365.

Kato F. 1991. Life histories of Masu and Amago salmon (Oncorhynchus masou and

Oncorhynchus rhodurus). In Groot C., Margolis, L. eds. Pacific Salmon Life

Histories. UBC Press, Vancouver. Pp 447-520.

Kostow K. 2003 Factors that Influence Evolutionarily Significant Unit Boundaries and

Status Assessment in a Highly Polymorphic Species, Oncorhynchus mykiss, in the

Columbia Basin. Oregon Department of Fish and Wildlife Information Report

#2003-04. Oregon Department of Fish and Wildlife, Fish Division, Portland OR,

USA.

Lenormand, S., Dodson J. J., Ménard A. 2004. Seasonal and ontogenetic patterns in the

20

ICES CM 2009 /H:06

migration of anadromous brook charr (Salvelinus fontinalis). Canadian Journal of

Fisheries and Aquatic Sciences. 61: 54-67.

Maekawa K., Nakano S. 2002. Latitudinal trends in adult body size of Dolly Varden,

with special reference to the food availability hypothesis. Population Ecology 44:

17-22.

McPhee M.V., Utter F., Stanford J. A., et al. 2007. Population structure and partial

anadromy in Oncorhynchus mykiss from Kamchatka: relevance for conservation

strategies around the Pacific Rim. Ecology of Freshwater Fish 2007: 16: 539-547

Morasse S., Guderley H., Dodson J.J. 2008. Paternal reproductive strategy influences

metabolic capacities and muscle development of Atlantic salmon (Salmo salar L.)

embryos. Physiological and Biochemical Zoology 81: 402-413

Morinville, G.R., Rasmussen J. B. 2003. Early juvenile bioenergetic differences between

anadromous and resident brook trout (Salvelinus fontinalis). Canadian Journal of

Fisheries and Aquatic Sciences. 60: 401-410.

Nordeng H. 1983. Solution to the "char problem" based on Arctic char (Salvelinus

alpinus) in Norway. Canadian Journal of Fisheries and Aquatic Sciences 40:

1372-1387.

Nosil P., Egan, S.P., Funk D.J. 2008. Heterogeneous genomic differentiation between

walking-stick ecotypes: “isolation by adaptation” and multiple roles for divergent

selection. Evolution 62: 316-336.

Olivieri I., Michalakis Y., Gouyon P-H. 1995. Metapopulation genetics and the evolution

of dispersal. American Naturalist 146: 202-228.

Olsen J.B., Wuttig K., Fleming D., Kretschmer, E.J., Wenburg J.K. 2006. Evidence of

partial anadromy and resident-form dispersal bias on a fine scale in populations of

Oncorhynchus mykiss. Conservation Genetics 7:613-619.

Olsson I.C., Greenburg L.A., Bergman E., Wysujack K. 2006. Environmentally induced

migration: the importance of food. Ecology Letters 9:645-651.

Olsson I.C., Greenberg L.A. 2004. Partial migration in a landlocked brown trout

population. Journal of Fish Biology 65: 106-121.

Pascual, M. A., Bentzen, P., Riva Rossi, C. M., Mackey, G., Kinnison, M., Walker, R.

2001. First documented case of anadromy in a population of introduced rainbow

21

ICES CM 2009 /H:06

trout in Patagonia, Argentina. Transactions of the American Fisheries Society

130: 53-67.

Piché J, Hutchings JA, Blanchard W. 2008. Genetic variation in threshold reaction norms

for alternative reproductive tactics in male Atlantic salmon, Salmo salar.

Proceedings of the Royal Society B- Biological Sciences 275: 1571-1575.

Ricker W.E. 1938. Residual and Kokanee salmon in Cultus Lake. Journal of the Fisheries

Research Board of Canada 4: 192-217.

Rikardsen, A. H., Svenning, M.-A., Klemetsen, A. 1997. The relationship between

anadromy, sex ratio and parr growth of Arctic charr in a lake in north Norway.

Journal of Fish Biology 51, 447-461.

Riva-Rossi C., Pascual M.A., Babaluk J.A., Garcia-Asorey M., Halden N.M. 2007. Intra-

population variation in anadromy and reproductive life span in rainbow trout

introduced in the Santa Cruz River, Argentina. Journal of Fish Biology 70, 1780-

1797

Rowe D.K. Thorpe J.E. 1990. Differences in growth between maturing and non-maturing

male Atlantic salmon Salmo salar L. parr. Journal of Fish Biology 36: 643-658.

Roff D.A. 1996. The evolution of threshold traits in animals. Quarterly Review of

Biology 71: 3-35

Schuster S.M., Wade M.J. 2003. Mating systems and strategies. Princeton University

Press, Princeton.

Taborsky, M. 2008. Alternative reproductive tactics in fish. In Oliveira, R.F., Taborsky

M., Brockman H.J. eds. Alternative Reproductive tactics: an integrative approach.

Cambridge University Press. Pp 251-299.

Thériault, V., Dodson J.J. 2003. The role of size in determining anadromy or residency in

brook charr (Salvelinus fontinalis). J. Fish Biology 63: 1-16.

Thériault, V., Garant, D., Bernatchez, L., Dodson, J.J. 2007. Heritability of life history

tactics and genetic correlation with body size in a natural population of brook

charr (Salvelinus fontinalis). Journal of Evolutionary Biology. 20: 2266-2277.

Thériault V., Dunlop E., Dieckman U., Bernatchez L., Dodson J.J. 2008. The impact of

fishing-induced mortality on the evolution of alternative life-history tactics in

brook charr. Evolutionary Applications 1: 409-423.

22

ICES CM 2009 /H:06

Tomkins J.L., Hazel W. 2007. The status of the conditional evolutionarily stable strategy.

Trends in Ecology and Evolution 22: 522-528.

Yamamoto S., Morita K., Goto A. 1999. Geographic variations in life-history

characteristics of white-spotted charr (Salvelinus leucomaenis). Canadian Journal

of Zoology 77: 871-878.

Yamamoto S., Morita K., Koizumi I., Maekawa K. 2004. Genetic differentiation of

white-spotted charr (Salvelinus leucomaenis) populations after habitat

fragmentation: Spatial–temporal changes in gene frequencies. Conservation

Genetics 5: 529-538.

23