GENE POOL CONSERVATION

Con~ewation is charged with thepresetyation of a dynamic, ever. changfng system of vanafron contained in each species.

Hampton L. Carson

Modern eenetics (the stu ~dv of hereditv and variation) has reached into every corner oi biology, d ras~ i&l l~ changing old-fa\l:ioned concepts. One set of new discoveries has to do with the existence of generic variation from individual to individual in natural ~~lpulat ionr . The natural pwu!ation of the human species displays suchvariabilliy, and it is not hard foithe casual observer to recognize that both genes and environment are involved. Some domestic animals (for example, dogs and cattle, Canis familiari.7, Bas taurus) also show easilv observed individual neneticvariation. This is an old storv: inf&mation frjm the n& &eneri&eClend.: bur perception and indicates (hat nearly every normal, sexually reproducin~ species is re lete with genetic vartntion. much of it s t the molecular levcl. Alrhourli [idden from easv ohber- vntion. permanetit molecular variation from individh to individual is io all- pewasive throughout nature as to constit~te an nlmoht un:\'ersal law of life.

In the last Century, wild animals and plants were frequent2 viewe? as if the individual members of a species were basically identtcal. ach mdividual was expected to conform to some kind of type; any deviation from the type was considered somehow unusual or accidental. The idea of twes is reallv a human concoction used to simpl~fy the way we deal with natuii. Fxcept pkr- haps as a device for cataloging material in museums, we mutt ab:indon the conccpt of the type, since gcneticq has shown it to he bad biology. We now know that not only is each human individual unique both in genetics and environment, but so is each dog or elephant or oak tree.

It is imoortant to recoeniz; that the conservationist is not chareed with the prese&ation of types. Indeed, what is out there in nature is a dynamic, ever-cliangin~ sptem of variation contained in each species. It is this flexible vGiaiiin svstem that lies at the heart of each of the oreanisms that -- wc study or va!uc ss something to be preserved. As contempo;ary biologist\, u e arc view~ng the systcm at only one moment in the progre.;? of geolopcal time. The co6servaiionist must iraoole with the difficultidea of ihe non- permanent n m r e of horh the sp'kciei and the ecosystem in which it exists. Although some species and ecosystems are more stable than others, ewlu- t i o n a ~ ~ c h a n ~ e wlth time is alaw of life.

Gkneticiariation arises through continual, irreparable, mutational changes in the D ? A carried in the cells. Most of these mutations have on1 a smal effect indtv~duallv: the eenetic uniaueness of individual.; is eenerarc (I" bv genetic recombination: i h i s 7s the naturally occurring ~crambling~rocess

118

tI1;tt the genes undergo each time the sex cells, egg and sperm, arc produced and then combined to form a new individual. Genetic recomhinat~on is a nearly universal accompaniment of sexual reproduction. which is the renro-

~ - - ~ ~ ~ ~ ~

ductive mode of almosi all of the forms of lifk that we mav un.ch to m n & G - ----, . . ---. -- - - .- -. . - . Some species, particularly among plants, have developed a capacity for clonal reproduction, in which a little piece of the mother plant becomes seoarated. as, for exam le, in a propagated cutting., The pie& can be induced io grow' into a new p 7 ant that is truly genetically den tical (except for new mutations) to the plant from which it was taken. A single mother plant can be used to make thousands of such cuttings. When planted out in afield. the r~wl t ino - . - - . - - - . -.. . plants may ]oak like a population, hut t h i colleclion does not have the varr ab~lity of a population; ~t is re:dlv only one 1n(l1\,1dua1. Cloning. procedures are wholly impractical as a means for conserving gene nook: th& can merely perpeiuate one or a few combinations of genes; mo&fiedon& slightly by the accumulation of non-recombining new mutations.

THE NATURAL POPULATION AND ITS POOL OF GENES

The discoven, of extensive genetic variation in natural ~ooulations led the , , ( ~ ~ ~ - ~ ~ . .... early pop~~lation genelici.;tr to &fer to the gcrictic m:lterial carrled by the individuals of the population a< a 'pool i r f genes. Ihic term is used to sug- zest the fact that a t ~ e uo~ulation-has a so? of collective hereditam endcw- - , ~ ~~

men1 that hclongs to thi bieeding group. In a sense, each time reproduction occurs, the individuals pool their genes i n the mathematical sense. It is from this pool that the next gcncrarim I I ~ intli\.iduals derives its genetic endowment. Ai long as the population of a zpecies remains large, natural selection will tend to preserve gcnctic variahilit) :n the gene pool.

POLYMORPHISM UNDER NATURAL SELECTION

Contram to earlier views. variabilitv in the eene 0001 does not consist of just :I small ;lumber of variabie genes of major gffect'scattered within a mostly 1111iil)rm. or homozygous, hackground. In contrast, the heterozygous state is the rule almost throughout the DNA. Most of the effects of these genes in hnth natural and artificial populations, furthermore, are individually small. Thic does not mean that they lack importance, however. Early in this century i t was ertahlishcd that most of the adantivelv imnortant characters of hoth plant, and animals (called the quantitbtivefharierers) are polygenically c~~ntrolled, mean~ng that many aenes of individually small effect contr~bute to each im~nrtant Aaracter. 'Thus. there is an additive as well as an inter- active som'poncr~t, and each character is affected bv many genes. This impor- tant f:wt ha\ heen somewhat concealed by the preoccupation of the human mcdlc;tl genetic~st with genes of large effect. These,are mostly serious acciJcnr;d mutations, amountin to defects in funct~on or structure; almost a11 are pathological in nature. -8, ey are not the raw matcnal that natural selection used to huild the human genotype. 'lhc importance ofthe small mutation was the original discoverv of the experimentd animal and plant breeders, who demonstrated the effects of artificial (man-induced) selection through their studies of the inheritance of quantitative characters. Natural selection is not different from artif~cial selection in itc basic attrihutes.

Gene Pool Conservnliott \Carson 120

Accordingly, the hreeding process in both natural and art~iicial populartons tends to Dreserve complexgcne comhinations that serve the needs of the nr~anism(or the ~raciical breeder) best in the heterozveous state.

At repmducth , the exist in^ gene comhinations aiereshuffled. and novel combinanons. perhaps only slightly difierent from thcir progenitors, are eenerated. These genetic refinements are continuallv being tested in natural - populat:ons. Con&rsely, recombinations prod~.cing blocks-oi gene. in the hnmozvgous state tend to have a lower fitness. so that population s u ~ v a l comes to depend more and more on individuals that are comolex multieenic heterozygotks. The result is what is called balanced genetic ~ l y m o r p h h n , a cond;tion [hat ?,sentiall) assures the mainten:lnce of eutcnsiw genetic variabilitv. At the same time. however. the svstem exacts a ~rice.since the individuds in the arc quite uneq;al in their cap~citv io produce progeny. The price consists of the necessary production oi a number of gene combinations that are relativeh inferior rer~roducer\. Scw laree or conwic- uous mutational changcs are in most case\'deleterious and are>limmate* by selection; or (as i n the case of industrial melanism in moths, for emmple) they are retained in the presence of many other gencs ofsmall effedt that have hcen selected, so that they modifv and refine the biological properties of the main biological charaster (in this cue , protective n~imicrv). There is no such thing as "5ne gene, one adaptation."

The non-geneticist tends to interpret the above emphasis on hetero- zygosity as meaning that ,qn~ and an heterozygosi must be preserved at any cost in order to kee apopulation genetically hezhy . However, the main- tenance of specific " % alanced heterozygosity' which serves the needs of the individuals in the populations is the crltical point.

ROTIXENECKS OF I'OPULA'I'ION SIZE AS GENETIC THREATS TO SURVIVAL

When a natural population is large, balanced polymorphism is main- tained by natural selection, and therc is usually m p l e opportunity for the fine-tunine nf the eenetic bxis of both adaotation to the environment and rcProductLe eff ic 'kq. A, was ment,oned above, the raw marcrial. that are incorporated are mostly genes of verv small individual effect. When the size of a natural ~ooulat ionb~comes reduced. however. the eenetic variabilitv on which the fldxibi~it~ of adaptive properti& depends mayYhc partly loht, o i the organization of i t mav he dkturhcd due to chance loses.

- Reduction in ~ouulation size constitutes a threat to the ~ooula t ion and this is manifested in ;ever31 wap. In clas3ical population &neiics, emphasis was placed on loss of geneticvariability due to the fact that breeding from only a mal l nurnher of individuals introduces a sampling error of reproduc- tion, such that some cne5 in low frequency in the parental population may hc h b.v chance from t i e descendant population. Such a loss is termed random drift and ha.. often been referred to as the Sewall Wrieht effect after its " discoverer. .~ ~. ~~ ~~.

Drift is surely an important source of variability loss, hut ,uch hottle- neeking, or unrepresentative constriction, of a population also has a disturb- ing effect on the genic equilibrium that underlies adaptive characters, cdus- ing genetic balance to undergo an equilibrium shift. The smallness of the, population provides less room for thc acc~immodation of the proce\s of trial

Gene Pool Coflservation \Camon 121

recombination. The system of adaptation is blind to what may be needed in the environment, so that when the population's ability to generate lots of variants is impaired, this also adversely affects adaptive response. In brief, a good adaptwe response and efficient reproduction of a population depend on the maintenance of balanced genetic polymorphisms. This balance 1s up- set in populations that have been reduced to a small size.

Following a population bottleneck, several outcomes are possible. The first, and the one that concerns the conservationist the most, is that the pop- ulation may be threatened with extinction. Some of the genetic details that underlie the death of a population or species are well modeled in what hap- pens in experimental populations and will be considered below. Basically, there is a loss of both genetic variability and its organization. If the reduc- tion in p<~pulatiun si&is nioderm, th& m:lv be &rely a shift from 3n older halanced condit:on 111 an dtered one. The nesr hdlance m3y serve the popul;~. tion equally uell. or i t inay pcrmit the urganim to better meet a ncw ecologi- c;tl challenge that might been instrumer~tal in the population decline. In such a c;ise. the genetics o i t l ~ c population chan~es to rncr.1 the changed cun~li- t i a m fulnu,~ng the hottleneck. Such genetic shifts mov ucc.lr rclativcly quicklv hut are not very diifcrent from .imil:~r b;~lt,ilce shift> that occur i n

larger pop~.liltions. I n sumc csset, howe\,er, the altered population mnv shou new conspicuou\ charxters (ior extmple, size, color of hmr) that reflect the underlying genetic shift. Indeed, s thcury of species forniat~tm has heen de- wluped around this ~~hcnomcnl~n of genetic reorg3nizatinn b recomhins~i~m.

In mnmaty, drastic red~~ctic~n i n populxiun sile nit,) be 7 olloncd by: I ) an apparent nm;~inten:~rii~~ uf the .srurrr.\ qiro; 2) 4 wdrlcn ~hi i t in impur- tant chttracrer,; or 31 cwtincti~m. Extinction is ccrt:~inlv h\ idr the must probable outcome of severe population bottlenecks.

THE GENE POOL OF ARTIFICIAL OR CAPTIVE POPULATIONS

The r.onsc.nutioni>t is pr~niarilv concerned wi th popu1;ttions cxist~nd in a .itsre of n:tturc, and t l i i b is the rearon for the cmpha~t\ placed ahwe nn natural populations. On the other hand, there a?e noGan increasing number of instances where the sizes of the natural nooulations of valued suecies have , , hecome so low that speci:,l or e\trhurdin:lry measures ;,re ireq~en'tly propth.4 for saving them. I'rumincnt :mmg these is thr. remwal of all specimens from nature and re.wrting. at 1cad teml1~3rily. to p rop~g~ t ion i n captivitv. Ex- amples arc the ('3lifornia condor and the 1lhnaii;tn crow ( G w ~ r n o ~ p \

T h e cxpcctcd genr.tic reil.lr< of cnptiw breeding or [~ ropag :hn are hrietlv outlined IieIu~.. The geneticist is in a reasonahl!. good pobitiun to make judgments on such procedures, since there is an exiensive literature on the eenetlcs of artificial oooulations of domestic animals and olants. includ- ing &ensive experimcnial'\rork on lrlhnratnq pn~~ula t iun~ u<~n,u,l)liilo (fruit or pumxe f l~e t ) , mice. :mi other species. Cunsider;~hlc evidence exist> Illat one uf the in;tjor pruhlcins ariring in m:Jl c:tpti\e populations is hreak- duun in the mating s!steni,; this >criously interferes nit11 the reproductive process. I n some birds :d insects. mide choice (either fem;~le choice or 1 1 1 . k choice) depends on the e\i>tence o i a genetic;~ll! v;tri:~hle field ui indi\.idu;lls that 3re suhject to the t)stein oiclioice. Such iid& of mating clmice

Gene Pod CONm6on I Guson 122

naturallv tend to be large (for examole, mating swarms of male flies such as midge,): if reduced in &e, repruduitive etiici:ncy appears to iall off. When captive populations are very small, the tendency exists for the popula- tion manager to bubsrit~te hislher oerson:~l choice oimates for a naturd one.

Sexnai selection. ooeratide thrbueh mate choice. is a oowerful svstem for efficient reproducti'on t h a t y e ~ i s yo maintain genetic halance, hitern- zygositl, and wgor in populations. In some expcr~mental populations of inxects opert~ting under sexual vAection, one-third of the males arc far more suecedul in reproducing than the other two-thirds. Were the opulation to he reduced by chmce to just a few males from the less succes.;t!l cnte ow a subsequent decline in vigor of the populathn wnuld iollow. Choicc oka il\gll- fitnesr male from a field ofgenetically vari3blc males is strongly indicated in i hex caws. l i the iield nimdes from uhich to choosc is spsrse, the female mav eo unmated even though what amears to the obselver as "eood" males ;ire br&ent. l'hc irrqul:lr siccess of piir matlngs in such ca,es also related to the phenomenon of female choice. Success of captive breeding programs in hirih, for example the condor and the 1 hw:,iian crow, :,re likely to run into difficulties of mate choice.

The above ohservatiorls suggest that, in breeding program>. every effort should he made by the managers of the populations to allow the natural cholce sptem that has e\olved within the specie. to opcratc in the ex lerimenul program. 'I'he females of many specles are far hettcr judges 0 / the reproduc- tive value of the different males that mav he availa5le than is the human manaeer.

6 e mdte choice principle, although probdhly very w~despread in animal. and to some degree in ulants. shnuld not he a w m e d to lx an absolute rule for the matine 6f all cabtive soecies. In the case of some rare unmlates in - ~. - ~~ ~

zms, tor exmple, a crafted progani of ni:de select~m b;,;ed on known xncc,. try mav be a necessav suhstitution for free mating choice. Such a rogram uas ormoscd h\ Temdettm (1950) and r~~ccei~fullv imolemented r or thc m:,li. ngemeni of the h r ee thg rem;lant bf speke's galelk (doze//o spekei) in zoos, where Lery ieu male. were avail:lble. Eswntisllv, the scliemr call, for rxtsi- tive artificial selection favorine a novel genetic &em in soecies that can uithstmd close mating of relaikes (inb;&ling).' Such s;hkmcs can be instituted, however, only in certain sprci 't I casts.

At this noint. it i, rele\.ant 111 recmoh:i\ize that the nrincinal chanec that is induced by a hottleneck in populatinn size i:. in or dnizatioc f . : Disorpnization ir not necersarilv lethal to the population. hus, .I shlft in genetic oreanization mav result once a oooulathi has successfuliv survived a critical lo;; of its origind genetic orr:in;z:;tion. A rrorg:mizetl chbracter may emerge in a few eener;~tio:is. l ' l~is nl~\.el cliaracter m w thus be imlmec! on The o o d a t i o n bv an altered orocess of selection that oderates on thk ~ ~

disorg;;ni;cd genttit rcmn:lnts t;i the former orqani/;ltlon.' A st~br~opulation derived in this manner is frequently much less vigorous

than the okiehal one. because of the nhase of imbalance through whi& the population must go Gelore natural seiection produces a new hdance. in very extreme ca,cs o i popolatinn SIX red.lction, where the new popdatmn ctems from one or vervfew foundinz individuals. it has been o ro~o i ed that an active period of d i rec tha l ic.lectio<may temporaril~ replxe'the'former Ihalancing selection. If the population can survive this, the result, aiter a series of gcn- erations th;it a l l w thc ooriulari~~n size to huild uo :wain. mav he mmifcsted in a population with a altered gene pbolr ~nshoi t , such a series

Gene Pool Conservation \ Carson 123

of events has been pro~osed as a mode wherebv new s~ecies evolve: however. shifts induced in 'x~)criment;tl p ~ ~ ~ ~ u l a t i o n s are hot thi<ir,~found.

Artificial breeding hyslcms are attempts to suhstit~te a new gcnelic \ywtn for the one that exided in thc nxtural ~onulation. 7'hi. is a tall order. and success in such a venture also has a There can be a substantiailoss of certain very desirable characters. For example, female choice among bower birds (Ptilonorhvnchidae) or birds of ~arad ise (Paradiseidae) d e ~ e n d s on vew elah~rate se~ondilry S P X U ~ I characte& o i male;. In nature, (he forest has many wni,peting malt$, caih d iq~lq ing ch3r;lctr.r that appeal not only to r h ~ reproduct~\e t ~ e s of the ierncile> hut s l v ~ to the human observer's aethctic sense. lJnder engineered programs of inhrrcdin~, :~ssuming that they would work, such I;~;c~~iating plumage and hehs\,ioral character, ~ o u l d he expected to erode under artificial \ ~ h ~ i o n to a n t ~ ~ r e munhne set of charmers. \Vh:,t i\ happening eenelic:tllv i.; t l i ; ?~ lhe m;ln;tger or hrceder i h ewlving a genetic +stem u hich he finds 'n~:~n:~ge;~hle, ' l'lic pop~~I:~tion that ix ultini:ttely t~re\en.cd m:n he hii~lu~ic;~llv far di>t;~nt irom the orizin:J a~;il.i of the - . - - preservation program.

CONSERVING THE GENE POOLS OF HAWAIIAN SPECIES

some other ipe&, not strongly developed. h he mating of close relatives seems not to be deleterious, nor has any clear loss of vigor followed in- breeding. Indeed, the breeding of close relatives may be natural to this species, making genetic management of small populations a relatively easy matter. Possibly, because of the history of repeated founder effects in the evolution of Hawaiian suecies. the conservationist mav be dealing with genetis h!htenir that h:~\h h~~ilt-in mech;~ni.;mi to p r e s k e genetic\wiahilit!, evcn i n p ~ p u I : ~ t ~ t ~ t ~ > that arc ireq~tently whjested to $e\ere reductionr or bottlenecks through a few individuals.

This t w e of oreadaotation exists in some terrestrial s~ecies naturallv dispcrxd \,;;>I arc:,; of open ocean. Some of the n a t h hcach plank of lldndi'i, tor eumplc. :Ire adaptcd to long-disttrnce di5persal and show littlc tendcncv 10 vay ctrsst~c;~ll! iruni island to i\land. I-ittlc 1s known of prop- erties of genetic h;,l:~nx, hut amne scem likelv to he adapted for the capaciry to reprod~ce after arrival hv onli ;1 single pr~ll~ngule, eifectively h\pdhsiny normal outcrossed sexual reuroduction.

exce6tion rather than the rule. It is possible to end this brief account on the following positive note.

Since most Hawaiian organisms have a long history of going through bottle- necks, there may be some degree of built-in ability to withstand the

Gene Pool Consen~a~iort\Camon 124

increasingly severe population bottlenecks now being imposed by widespread environmental destruction. Verv few soecies. however. can be successfullv pro agared in the lahoratory, f'eid c x p e h e n t a l farm, or mo. l'hei; ecokgical requirements are often too spectal. Only a minority of Hawaiian Droso>hila soecies. for examole. can bebred in thelaborator? even for those'that can he so hred, iniportant natural characteristics a ie evidently 10% Shture is ;I better stockkee er than we are, and this principle would appear to apply to many kinds oforganisrns. From the gm& point of view, the estahlisllment of manv rehtively small reserves ma!, serve ar viable reiugia ior I lawaiian plants and an~mals. &e size of a successful rehgiurn in Hawhi'i should be determined by what it takes to provide maximal insula- tiun of [he ecosystem from encroachment b aliens and to rotect it from other adjacent degrading forces (see also d l t , this volume!. A large number o i refuria of ec~~loeicnllv sound size will ~ robab lv serve Hawaiian consewa- tion needs better than <fewlarge areas.'

Important References

Carson. H.L. 1986. Patterns of inheritance. American Zoolopisl 6797-8(n. Canon. ILL. 1987. The process wbcrcby species originate. B;nrctenre 37(10):715-720. Cmant, 5. 198.8. Sdving cndangcrcd rpecie, hy trmslou1i.m Biorrmcc 38(4):254-257. Frankel. O.H.. aod M.E. SoulC. 1981. Conremation and Evoi:dion. Cambridec Uniwrritv

press, &bridge, England. -

He- J.P., and J.K Hodges (eds.). 1985. Advonces in Animal Conse~ t ion . Clarendon Press, Oxford, United Kingdom.

Holl, A. [This volume] Protection of nahlral habitats. Schanewald-Cox, C. 1985. Genelieg minimum population size, and the island prexrvc.

Pp. 432458 IN C.P. Stone and J.M. Scott (eds.),Hawoi'i's TerresrriolEeosysrems: Premvarion andManogenmrr. Univ. Hawaii Press Tor Univ. Hawaii Cooperative National Park Resources Studies Unit, Honolulu.

Scbonewald-Cor, C.M., S.M. Chambers B. MacBryde, and W.L. Thomas. 1983, Generics and CmeIyalion: A Reference for Manoninn Wld Aninlo1 and Pbnt Pomloriom. - " Benjamin/Cummings Publ. Co., Menlo Park, California.

Soul4 M.E. (ed). 1986. Cow-ti01t Riolw: The Science ojScarciry andDiwmiry. Sinauer Assc&tes. Inr. Sunderland. h & a c h u ~ t t r . .

Templeton, A.R. 1980. A theory of speciation via the founder principle. Genetics 941011-1W.