the evolution of live-bearing in lizards and snakes

8/13/2019 The Evolution of Live-Bearing in Lizards and Snakes

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The University of Chicago

The Evolution of Live-Bearing in Lizards and SnakesAuthor(s): Richard Shine and J. J. BullSource: The American Naturalist, Vol. 113, No. 6 (Jun., 1979), pp. 905-923Published by: The University of Chicago Press for The American Society of NaturalistsStable URL: http://www.jstor.org/stable/2460311 .Accessed: 28/08/2013 23:52

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Vol. 113, No. 6 The American Naturalist June 1979

THE EVOLUTION OF LIVE-BEARINGINLIZARDS AND SNAKES

RICHARD SHINE* AND J. J. BULLDepartment f Biology, University f Utah, Salt Lake City, Utah 84112

Most reptiles ay eggs, but many izards nd snakes are live-bearers. axonomicand embryological vidence ndicates that egg-laying s ancestral Weekes 1935;

Matthews 1955; Amoroso 1960), so the common occurrencef genera containing

both ive-bearers nd egg-layers hows that ive-bearing as arisen from gg-layingseveral times table 1). This paper considers he ecological conditions avoring heevolution of live-bearing n squamate reptiles. here have been several excellenttreatments f reptilian ive-bearing hich have made this urrent ynthesis ossible(Mell 1929,Weekes 1935; Sergeev 940; Neill 1964,1971; Packard 1966; Greer 1968;Fitch 1970; Greene 1970; Packard et al. 1977; Tinkle and Gibbons 1977). Here acomprehensivemodel is presented o account for the evolutionary rigin of live-bearing, nd published ata are used to test predictions rom he model.

ORIGIN VERSUSMAINTENANCE

The evolution of live-bearing rom egg-laying n squamate reptiles s almostcertainly gradual process. n the early tages of this process, emales arry he ggslong enough to permit ome embryonic evelopment n utero but ay the eggs priorto the completion f mbryogenesis. ontinued election or rogressivelyonger ggretention ventually esults n complete ntrauterine ncubation live-bearing).

Certain physiological nd anatomical changes must accompany the transitionfrom gg-laying o live-bearing Weekes 1935; Bauchot 1965; Yaron 1972). Theserequirements robably prevent ny rapid evolutionary jump from egg-laying(without n utero development) o live-bearing. or example, the female mustdevelop vascular structures or gaseous exchange between viducts nd offspring,and she must maintain nly a thin egg shell around them whilethey re in utero.These modifications ust be more xtensively eveloped n females hat retain ggslong time than n females hat retain ggs only a short ime, ecause the need forexchange between mother nd offspring ncreases s the embryos become larger(Dmiel 1970).Thus, even females apable of retaining ggsfor hort ntervals re notnecessarily apable of sustaining ggs n utero hroughout evelopment. ackard etal. (1977)also provide upporting vidence for hese ssumptions.

In order for live-bearing o arise from egg-laying, election must favor theintermediate tages n which females etain ggs for progressively onger periods of* Present ddress: Zoology Department, niversity f Sydney,New South Wales 2006,Australia.

Am. Nat. 1979. Vol. 113, pp. 905-923.?C1979 by The University f Chicago. 0003-0147/79/1306-0009$01.65

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906 THE AMERICAN NATURALIST

time.There may be circumstances n which t s advantageous o be live-bearing, utin which the intermediate tages of egg retention re not favored Weekes 1935;Tinkle 1967; Packard et al. 1977; Tinkle and Gibbons 1977). A major differencebetween live-bearing emale nd an intermediate gg-retaining emale s that thelive-bearer s emancipated rom esting while the ntermediate emale s not. f theact of nesting s strenuous r risky, hen n advantage ccrues o live-bearing ut notto the ntermediate tages of ggretention. n discussing he volution f ive-bearingit is therefore ecessary o distinguish orces whichprovide n advantage for heseintermediate tages i.e., favoring he origin) from orces which merely rovide nadvantage or he maintenance f ive-bearing. his paper nvestigates nly he originof live-bearing. he maintenance f live-bearing s considered by Sergeev 1940),Tinkle and Gibbons (1977),and Shine and Berry 1978).

ECOLOGY

How will selection ct upon a female arrying er eggs slightly onger han theaverage female, husallowing heyoung o develop n utero nd spend esstime nthe nest? The fitness arametersmost ikely obe affected y oviducalretention re(1) offspring urvival, nd (2) mother urvival nd future ecundity. gg retention smost ikely o be favoredwhen ither i) the urvival f young sgreatly mproved yoviducalretention, r ii) the mother oes not ower her future ecundityf he carriesthe eggs onger Appendix). ome ecologicalfactors hich may favor ggretention n

these ways are discussed below. Also, we attempt o distinguish actorswhich anselect for he complete volution of live-bearing rom actorswhich electonly forshort ntervals f egg retention.

Factors Affecting gg Survival1. Temperature. Proper embryonic evelopment n squamate reptiles equires

limited angeof temperatures, nd temperature xtremesmay be fatal Fitch 1964;Licht and Moberly 1965; Vinegar 1974).Also,the rate of embryonic evelopment sproportional o temperature n some species Blanchard nd Blanchard 1941;Fitch1954; Platt 1969). The fitness f hatchlings herefore epends upon incubationtemperature o the extent hat embryogenesis ust be normal nd hatching ccursduring omeoptimal ime.Certainly hemother hould ay eggs n the ites which remost thermally uitablefor evelopment, ut some environments aybe so extremethat ideal nest sites are not available and eggs will inevitably e exposed tononoptimal emperatures. uch thermal nsuitability ay be.characteristic f coldenvironments nd possibly f hot environments.

Cold environments may adversely ffect he fitness f hatchlings or the tworeasonsoutlined bove: (a) The nest ubstratemay be coldenough o harm mbryos,

and (b) the cold nest may slowdevelopment o that hatching ccurs ater han omeoptimal ime.Thesetwo effects re not necessarily ndependent, ut the distinction suseful.As an example of (a), eggs might be laid early enough n the spring o besubjected o late frosts. or (b),montane nd some temperate nvironments ouldbetoo cool to permit pring-laid ggs to hatch ufficiently ong before winter.



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EVOLUTION OF LIVE-BEARING 907

Cold environments re unique in that short intervals f egg retention mayovercome thermal omplications uring development. n the example of (a), eggretention ould avoid exposure of eggs to the frosts, ince the mother ould seekshelter t frost-free epths. n the example of b), egg retention ould lead to earlyhatching f the mother maintained a body temperature igher than substratetemperature uring art of the day. When aid, embryos would be developed furtherthan f heyhad remained n the ground uring he same nterval. t is in fact nownthat females f some species ccelerate evelopment y thermoregulating hen heyretain ggs, nd thus hasten hatching Sergeev 940; Blanchard nd Blanchard 1941;Stewart 1965; Hirth and King 1969; Osgood 1970; Packard et al. 1977). Coldenvironments eed not always favor egg retention, hough. The time of hatchingcannot be hastened f the development ate s temperature-independent e.g.,Chely-dra, Yntema 1968) or if hemother maintains he ame temperature s the ubstrate(aquatic or fossorial pecies, Brattstrom 965).Cold environments hould therefore ften elect for egg retention, s suggestedpreviously Mell 1929; Weekes 1935; Sergeev 1940; Packard 1966; Greer 1966;Packard et al. 1977). n addition, old environments avor he progressive volutionto live-bearing ecause they often ccur as gradients romwarm to cold habitats,with atitude or altitude. As populations of individuals hat retain eggs becomeestablished n cool areas, selection an favor ncreased retention imes mong theinvaders f even cooler areas. This can progress ntil ive-bearing volves.

Temperature xtremes re less ikely o be a problem n hot environments han n

cold environments, ecausehot environments sually ontain many microhabitatsthat do not experience armfully igh temperatures. t is conceivable, hough, hategg retention ould evolve n response o rapid easonal changes n ground empera-ture, s in some deserts. A shallownest ufficiently arm n springmay become toowarm ater, efore atching. deep nest maynever ecome oo warm, ut could eadto late hatching ecause it is too cool in spring. ome benefitmay be derived romretaining ggs until the environment asses through he temperature luctuation.This does not seem as compelling cause for he evolution f egg retention r live-bearing s cold environments, owever.

2. Predation. Predation s a source of high egg mortality n many reptiles ndtherefore may lead to selection for egg retention. he benefit f retaining ggsdepends upon how predation s reduced by late laying nd less time n the nest.Conceivably, gg retention ould evolve n response o predation when the risk ofpredation s proportional o the time spent n the nest. However, vailable dataindicate hat predation s not proportional o the time of incubation. n the casesstudied, predation has proven to be high ust after he eggs have been laid, andpossiblyhigh when heyoung merge, ut predation may be slight n between Blair1960;Moll and Legler 1971;Carr 1973). Egg retention ill reduce predation nlyslightly nder hese ircumstances, ecause ts only ffect s to shorten he nterval n

which there s little mortality. With this form of predation ive-bearingwill befavored ver egg-laying, ut the ntermediate tagesof ggretention robably onferno advantage.

3. Moisture extremes. Some authors have proposed that the two extremes fmoisture ontent n the nest wet nd dry) elect or ive-bearing Weekes1935;Neill



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1964). Neill proposed that eggs aid in wet oil are subject o infection nd that hisselectsfor ive-bearing. ther possible reasons for mortality n wet or dry nests reconceivable.Unfortunately, o meaningful iscussion f these factors s yet possiblebecause little s known bout egg mortality n wet or dry nests. t is also difficult odraw correlations etween gg retention nd nest humidity ecauseinformation slacking n the nesting ites fmost pecies. A species hat ccupies wet habitat maybe able to locate dry nesting reas, nd vice versa. Even if wet or dry oil lowers ggsurvival, etention eednot be favored. etention hould volve only f hemortalityfalls hiefly n the early tages of embryogenesis, r on eggsthat remain n the nestslightly oo long. Otherwise reduction n time spent n the nest will not greatlyincrease gg survival.

There s one case in which hort ntervals f eggretention may evolve becauseofnesting n dry habitats. f a long dry season preceeds gg laying nd rain usuallycomes at the onset of nesting, hen t may be advantageous o delay aying until trains (Gehlbach 1965). Eggs are thus laid in moist soil, possibly ncreasing heirsurvival. Egg retention er se need not offer n advantage to the eggs,but if thetiming f the rain s unpredictable nd the mother must ay soon after recipitation,then early ovulation allows her the flexibility f laying at any subsequent ime(Stearns' bet hedging, 1976]).

Of the ecologicalfactorswhich ffect gg survival, cold environment s the mostappealing ause for he volution f ive-bearing. lthough here re many ources fegg mortality hich may be improved lightly y retention, old environments re

unique n that i) they an be lethal oembryos, ii) they an be compensated or yshort ncreases n retention ime, and (iii) they occur in graded lines, allowingprogressive volution o live-bearing. ortality ources which re proportional othe time pent n the nest do not have as high benefit/cost atiofor gg retention.

Factors Affecting heMother

A female aden with ggs s less efficient t locomotion nd, hence, may be morevulnerable o predators nd less able to forage han f he had laid the eggs Fitch1970; Tryon and Hulsey 1976). Egg retention s perhaps most disadvantageous omothers f species in which females move about actively fter aying ggs. f thefemale id not retain ggs, he could be moving bout and feeding ooner. However,there re many pecies n which he female oils around he ggs nd stayswith hemthroughout ncubation. These brooding females suallydo not feed during histime FitzSimons1919; Pope 1935;Fitch 1954; Sweeney 961; Taylor 1965; Leakey1969).Retentionmay not be costly o such a female, ecause t does not prolong heinterval n which he abstains from eeding.

1. No maternal are after aying. Perhaps the main cost of retaining ggs s the

mother's ecreasedmobility. his makes her ess able to feed nd morevulnerable opredation. Egg retention hould be least disadvantageous n species that are leastprone to predation r that do not depend on rapid movements or feeding. ive-bearing hould evolve most often n species that are (1) large and deadly, becausethey can ward off predators Mell 1929; Sergeev 1940;Neill 1964); (2) secretive,



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becausethey arely ncounter redators Mell 1929;Fitch 1970); or 3) slow moving,because they do not depend on speed to escape predators r to catch food Fitch1970). n contrast, rboreal pecies which ely n agility o feed r to avoid predatorsshould be at a greater isadvantage when retaining ggs.

The above comparisons ssume that females ontinue o move about and feedwhile retaining ggs. This is only ikely o be true for hort ntervals f retention.Females of many snake and lizard species become very ecretive nd curtail heiractivities hen arrying ggsfor long period, ven n large nd deadly pecies e.g.,the live-bearing nakes Vipera, Prestt 1971; Crotalus, Keenlyne 1972; Sistrurus,Keenlyne nd Beer 1973; Agkistrodon, itch and Shirer 971; Notechis, seudechis,Shine 1978). This tends to equate the cost of egg retention mong the differentspecies.

Retentionmight volvebecause of short-term vents hat ffect he ase and safetyofnesting. or species hat dig or construct ests mainly izards), ainmay facilitatethe construction f a nest n a dry rea. If nesting ccurs at the time of year whenrains begin, hen he female may be favored o retain ggsuntil ain falls Anderson1962). (Recall that egg survival may also be enhanced n this situation.) Longintervals f retention eed not be favored ince the advantage of waiting may beoutweighed y the disadvantages f ong-term etention.

2. Maternal care.-Egg retention may not be as costly o a mother f he broodsthe eggsfrom aying ntil hatching: y carrying he ggs onger, hedoesnot havetobrood them s long. This compensation means that egg retention s more ikely o

evolve n a brooding pecies han n anonbrooding pecies.Broodingmayevenfavor

egg retention, ut may not suffice o favor ive-bearing. uring the early tages ofdevelopment etentionmay be less costly han brooding, ecause retention llowsthe mother reedom f movement o feed.As the embryos evelop, he eggs ncreasein volume and weight, nd the mother ecomesmore heavily burdened e.g.,Fitch1954;Shine 1977).Eventually, t becomes dvantageous ocease moving round ndto lay the eggs.

Cold environments rovide n advantage for etention n a brooding pecies hatdoes not apply to a nonbrooding pecies. n cold environments he mother's ighbody temperatures an accelerate embryonic evelopment uring retention. hisshortens he total incubation period retention lus brooding) and therefore aydecrease the mother's otal interval f parental care. Live-bearingmay thereforeevolve from rooding n cold environments ven f egg survival s not affected.

3. Other revious ypotheses. ) Prolonged gg retention elays he ime t whichthe mother can ovulate her next clutch. This might be a major disadvantage nspecies hat ay more than one clutch er season (Sergeev 1940;Tinkle nd Gibbons1977).

ii) Two common arguments n the literature re that live-bearing volves inaquaticor arboreal pecies because the mother s freed rom aving o leaveher usual

habitat n order o find suitablenesting ite Mell 1929; Sergeev1940;Neill 1964;Fitch 1970). Clearly, his does not apply to the intermediate tages because themother till has to find a nest), and therefore ill not lead to the evolution oflive-bearing Packard et al. 1977).The arboreal habit may even select against theevolution f ive-bearing see above).



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TABLE 1

RECENT RIGINSOF LIVE-BEARING*

Proportion fLive-Bearing Maternal

Species n Care KnownFamily, Genus Cold Climates in Taxon? Authority

LizardsChameleontidae

Chamaeleo ........... 3/3 - Schmidt & Inger 1957Iguanidae

Corytophanes ......... 1/1 - McCoy 1968Liolaemus ........... 13/20 - Donoso-Barros 1966Phrynosoma .......... 3/3 - Stebbins 1954;

Lowe and Howard 1975Sceloporus eneus 1/1 - Davis & Dixon 1961;S.formosus roup ..... 2/2 - Stuart 1948;S. scalarisgroup ...... 1/1 - Fitch 1970;S. variabilis roup ..... 1/1 - Werler 1951

ScincidaeAnomalopus .......... 1/1 - A. E. Greer,

personal ommunicationEumeces ............. 3/3 + Axtell 1960;

Van Devender ndVan Devender 1975;Webb 1968;Legler & Webb 1960

Leiolopisma - Barwick 1959;(New Zealand) ..... 15/15 Cogger 1975;(Tasmania) ........ 5/5 Rawlinson 1976;

McCann 1955Leptosiaphos ......... ?/1 - Loveridge1942Lerista .............. 1/1 - Greer & Parker 1967Lygosoma ............ 0/4 - Greer 1977Mabuya South Africa). 7/10 - Horton 1973Mabuya Asia) ....... 1/1 - Smith 1935;Horton 1973Scincella ............. 1/1 - Smith 1935Sphenomorphus

(NewGuinea) ...... 2/3 - Greer & Parker 1974;Fitch 1970

Tribilonotus .......... ?/1 - Greer & Parker 1968LacertidaeEremias ............. 2/2 - Sergeev1940Lacerta .............. 1/1 - Smith 1973

AnguidaeDiploglossus .......... 2/4 + Greer 1967;

Taylor 1956;Lynn & Grant 1940

Gerrhonotus .......... 9/9 + Stebbins 1958;Greer 1967

AgamidaePhrynocephalus ....... 1/1 - Smith 1935;Minton 1966

(Continued)



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TABLE 1 (Continued)

Proportion fLive-Bearing Maternal

Species n Care KnownFamily, Genus Cold Climates in Taxon? Authority

SnakesTyphlopidae

Typhlops ............ ?/1 + Bogert 1940; Taylor 1965Colubridae

Aparallactus ......... 0/1 - Pitman 1974Coroniella ............ 1/1 - Smith 1973; Street 1973Elaphe .............. 1/1 + Pope 1935; Oliver 1959;

Fukada 1965Helicops ............. ?/1 - Rossman 1973

Opheodrys ernalis .... 1/1 ? Ditmars 1942Sinonatrix ........... 1/1 + Pope 1935; Smith 1973Viperidae

Cerastes ............. ?/1 - Domergue 1959Echis ............... 1/1 - Minton 1966;

Mendelssohn 1965;Duff-Mackay 965

Vipera .............. 3/5 - Mendelssohn 1963Crotalidae

AgkistrodonAsia) .... 2/4 + Pope 1935, Smith 1943;Wall 1921

Trimeresurus ......... 2/4 + Pope 1935; Fukada 1964;Nickerson 1974

ElapidaePseudechis ........... 1/1 - Covacevich & Tanner,personal communication

NOTE.-Symbols: + = yes;-= no; ? = insufficient ata.* Genera, pecies groups, r species containing opulations f egg-layers nd live-bearers taking he

smallest axon containing oth types) with ata on habitat, limate, nd maternal are in the taxon. Wehave omitted oubtful ecords Tinkle and Gibbons 1977; Spellerberg 976; Packard et al. 1977), andcases where ontinents ave been colonizedby live-bearers.

ii) Intermediate tages of ive-bearing. Many speciesretain ggs ong enough forembryonic evelopment o reach visible tate t the time of aying table 2). Thesespecies have progressed art of the way toward evolving ive-bearing nd shouldtherefore ndicate he ecological factors avoring heevolution f ive-bearing.

In order to test the hypotheses, e assembled ecologicaldata from publishedliterature or live-bearers with congeneric gg-layers nd for species with eggretention tables 1, 2). In addition, we gathered he same ecological data for over1,000 pecieswhich how neither ive-bearing or eggretention table 3). These atterdata serve as an estimate f the expected requencies f the various ecologiesforsquamates s a whole; they orm hebasis for esting or bias in the cologiesof helive-bearers nd egg-retaining pecies.The assignment f hese pecies othe different

ecological categories was based on ecologicaldescriptions n the sources table 3,footnote). n the absence of absolute definitions f cold climate,wet or dry habitat,and so forth, relative measure was used for these ecological categories n eachcontinental rea. This no doubt introduces ubjectivity nto these assignments, utno alternatives eempossible t present. incethe ests f ignificance re themselves



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TABLE 2

INTERMEDIATE STAGESOF LIVE-BEARING. SQUAMATE SPECIESWITH EGG RETENTION;DATA ON HABITAT, CLIMATE, AND MATERNAL CARE IN THE SPECIES

PopulationIn Cold Maternal

Family, pecies Climate? Care? Authority

LizardsIguanidae

Anolis aeneus ........... - Stamps 1976A. cybotes ....... ...... + - Huey 1977A. shrevei ....... ...... + - Huey 1977Liolaemusmonticola ..... + - Donoso-Barros 1966Sceloporus larki ........ + - Kauffeld 943;Stebbins 1954S. orcutti .............. + - Stebbins 1954; 1958S. scalaris ........ ...... + - Anderson 962S. undulatus ............ + - Gehlbach 1965S. virgatus .............. - Vinegar 1975

ScincidaeAnotismaccoyi .......... + - Pengilley 972Eumeces revilineatus* ..- + Werler 1951E. callicephalus* ........ + Campbell & Simmons1961;

Zweifel 962E.fasciatus* ............ + + Cagle 1940; Fitch 1954Leiolopisma uichenoti .. + - Pengilley 972L. suteri ............... + - Towns 1975L. trilineata ..... + - Pengilley 972Morethia oulengeri ..... + - Rawlinson 1976Scincella laterale ........ - Johnson 1953Saiphos qualis .......... + - Bustard 1965; Cogger 1967

LacertidaeLacerta agilis ........... + - Smith 1973L. muralis ............. + - Cooper 1965L. viridis .............. + - Marshall 1956

AnguidaeDiploglossus elasagra ... ? + Greer 1967; Taylor 1956Gerrhonotus ulticarinatus + - Stebbins 1954, 1958

HelodermatidaeHeloderma uspectumr - - Ditmars 1942,doubtful; ee

Bogert & Dal Campo 1956

AgamidaeCalotesversicolor ....... + - Muthukkaruppan t al. 1970Snakes

BoidaePython molurus ......... + + Pope 1961;

Van Mierop & Barnard 1976P. reticulatus ........... + Pope 1961; Fitch 1970P. sebae ............... + Joshi 1967;

Branch & Patterson 975.Typhlopidae

Typhlops iardi ......... ? Wall 1918, 1921; Smith 1943;Taylor 1965

T. schlegeli ............ + - FitzSimons 1962Colubridae

Ahaetulla haetulla ...... + - Smith 1943; Taylor 1956;Pope 1935; Wall 1921

(Contintued)



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TABLE 2 (Continued)

PopulationIn Cold Maternal

Family, pecies Climate? Care? Authority

Amphiesmatolata ....... + + Wall 1921; Minton 1966Amphiesma ibakari ..... + - Fukada 1956;Malnate 1962Aspidura rachyprocta ... + - Wall 1921Boiga trigonata ......... + - Wall 1921Carphophis ermis ....... + - Clark 1970Diadophis unctatus ..... + - Ditmars 1942; Blanchard 1930;

Fitch 1975Elaphedione* ........... + - Fukada 1965E. obsolete ............. + Ditmars 1942; Fitch 1970E. taeniuris ............ + - Pope 1935E. vulpina ............. + - Zehr 1969Helicops ngulatus ....... Rossman 1973Lampropeltis riangulum . + ? Ditmars 1942Lycodon ulicus ......... + + Wall 1921;Smith 1943Natrix maura ........... + - Duguy & Saint Girons 1966N. natrix .............. + + Angel 1950; Smith 1973;

Parker 1963N. percarinata .......... + + Pope 1935Opheodrys ernalis ...... + ? Blanchard 1933;Ditmars 1942;

Stille 1954;Minton 1972Pituophismelanoleucus* + ? Anderson 1965;Carl 1944Psammophylax hombeatus + + FitzSimons 1962Psammophylax ritaeniatus - + Sweeney1961Ptyas dhumnades ........ - Pope 1935

ViperidaePseudocerastes ersicus + - Mendelssohn 1965;

Minton 1966Crotalidae

Agkistrodon cutus ...... + - Pope 1935; Smith 1943;Leakey 1969

A. rhodostoma .......... + Smith 1943Trimeresurus onticola + + Pope 1935; Wall 1921

ElapidaeCalliophismacclellandi .. + - Soderborg 1973Micrurusfulvius ......... + Ditmars 1942;Mole 1924;

Campbell 1973Naja naja ..............- + Pope 1935;Campbell & Quinn 1975

* Egg retention nferred rom hort ncubation eriod < 26 days).

merely omparisons f frequencies, ubjectivity n the data does not influence heconclusions, rovided we have been consistent.

1. Live-bearingnd egg retention hould volve n cold climates If cold is a majorcause for the origin of live-bearing, hen the species or populations which have

recently volved live-bearing hould be found n cold climates more often hansquamates as a whole.This prediction s supported y the casesin table 1for whichhabitat nformation savailable 33 origins). Giving qual weight o each origin each-ntry ultiplied y the proportion f ive-bearers n cold) reveals hat 8.1 of 33 cases



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TABLE 3

DISTRIBUTIONS OF SQUAMATE SPECIES WITH RESPECT TO HABITAT AND OCCURRENCE OF PARENTAL CARE;PROPORTIONS IN EACH CATEGORY

Live-Bearers n Generawith Both Egg-Laying nd Species with

All Live-BearingMembers Egg RetentionSquamates (n = 38) (n = 60)

Cold climate ..................... .44* > .74 .72(.13-.61)

Wet soil ..12* .11 .13(.04-.22)

Dry soil ..18* .24 .05(.03-.35)

Aquatic .05* .03 .02

(0-.14)Arboreal .10* .08 .08(.02-.28)

Maternal are(at generic evel) lit .24T .33

* Based on data for 1,077 species from Africa, hina, Australia, nd North America, romPitman(1474), Pope (1935), Cogger 1975), Conant 1958), nd Stebbins 1966); brackets ive ranges f the fourcontinental means. Categories were determined y the respective uthors' criteria nd our personalknowledge f the speciesand habitats North America nd Australia).

t Based on data for 700egg-laying pecies 231 genera) n Fitch 1970).T In egg-laying orms.

(85%) are found n coldclimates. his s significantly ifferent rom he proportion nsquamates s a whole 44 %; Fisher's xact est, < 10- 5 ). Even f ll of he unknowncasesin table 1 are assumed o inhabit warm nvironments, heproportion f newlyevolved ive-bearers n cold climates 28.1 of 38, or 74%: tables 1, 3) is much higherthan among squamates in general (440%; P < .001).

Egg retention s also significantly orrelatedwith old climate: able 2 shows that43 of the 60 egg-retaining pecies are found n cold climates, while another 15(possibly 17) are not. Thus, the proportion f egg-retaining pecies found n coldclimates is significantly igher than that for squamates as a whole (72o%versus 440%;table3,Fisher's xact, < 10-4).2. Egg retention nd live-bearing hould volve more eadily n species with emaleparental care than n species without emale care. Egg retention hows a strongcorrelation ith brooding: 18 of 55 known brooding pecies 33 %) retain ggs,butonly 39 of 650 nonbrooding pecies 6%) have oviducal retention Fisher's exact,P < 10- 5). In addition, ive-bearing as arisen more frequently n brooding han nnonbrooding enera: Live-bearing as evolved n eight of the 15 brooding generacontaining more than one species 53 %),but n only 24 of the 150polytypic on-brooding genera 16 %). The difference n proportions s significant Fisher's exact,

P < .005).We must be cautious that brooding pecies are not disproportionately ound ncold environments, s this could account for part of the above correlations. We donot know definitely fbrooding s correlatedwith old,but the data in table 2 (here)



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916 THE AMERICANNATURALIST

and in figure of Tinkle and Gibbons (1977)suggest ot.This possible bias can becircumvented, owever, y restricting hecomparison o taxa in cold climates. f 13brooding genera with taxa in cold climates, ive-bearing as arisen n 7 of these(54

%),whereas ive-bearing asarisen n only 3%of he nonbrooding enerafound

in cold climates 23 of 101genera; able3 has only pproximations f thesedata). Ifwe assumethat he brooding nd nonbrooding enerahave had the ame number fspecies n cold climates equal opportunity or he origin f ive-bearing), hen hecorrelation s significant Fisher's xact, P < .05). Therefore, t seems that broodingenhances he evolution f ive-bearing s well as the evolution f egg retention.

3. Egg retention nd live-bearing hould ot volve nresponse o aquaticor arboreallife, r to extremes f soil moisture.-If hese habitats promoted he evolution oflive-bearing, hey hould contain many specieswith egg retention nd many ive-bearing pecies with gg-laying ongeners. able 3 does not support hisprediction.Species n these habitats have evolved gg retention nd live-bearing bout as oftenas would be expectedfrom heir proportions n squamates as a whole (P > .05 inall cases).

DISCUSSION

Live-bearing as evolvedfrom gg-laying ore han30 times n squamatereptiles.Severalhypotheses ave been presented ere o account for he origin f ive-bearing.The model we advocate assumes hat ive-bearing volvesfrom gg aying nly f he

intermediate tagesof egg retention re selected or. gg retention s a state n whichfemales elay aying nd carry heeggsto allow partial mbryonic evelopment nutero. f selection avors ncreasingly ongerperiods of eggretention, ventually hepopulation will contain femaleswhich give birth o live young. This model is notunique to our paper, but we have extended t as well as tested t.

Both theory nd data suggest hat two factors, old environments nd maternalcare of eggs, ndependently electfor ggretention. f these nly cold climate eemsto favor he full ransition o live-bearing; roodingmerely acilitates hetransition.Cold climate has often een proposed as a major factor avoring he evolution flive-bearing Mell 1929;Weekes 1935;Sergeev 1940;Packard 1966;Greer 1966;Packard et al. 1977).Sergeev vencontended hat old climatewas the singlemajorforce n the evolution f quamate ive-bearing, lthough e did not rule out all otherecological factors e.g., aquatic habitats), merely egarding hem as having smalloverall ffects. his study upports ergeev's ontention hat old is the major force,but his case can perhaps be made more strongly, ecause origins f live-bearingoutside of cold environments eem to be rare. A demonstrative ase is providedbybrooding,which readily eadsto eggretention. f many factors ven weakly electedfor ive-bearing, henwe would expectbrooding oenhance his election o that tleast some origins f ive-bearing ouldnot occur n coldclimates. et, t least ix of

the eight ecent rigins f ive-bearingn brooding enera havebeen n coldclimates,and perhaps ll of them re (one genus unknown, ne-half heexamples f anothergenus nhabit old climates).

We have emphasized wo somewhat ifferent easonswhy old may be important



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in the evolution of live-bearing: a) Cold may injure the embryos t the time oflaying; b) cold may slow development o that hatching ccurs ater han s optimal.Hypothesis a) requires hat ground emperatures t the time of ovulation must below enough to harm the embryos. his is directly estable on a species-by-speciesbasis, but there s no universal emperature minimum which can be consideredinjuriously old. Ground temperatures hich re lethal o eggs of a tropical peciesmay be warm by temperate tandards. or example, ggsof a tropical guana, whichdevelop normally t 300C, cannot tolerate ven a week's exposure o 200C (Lichtand Moberly 1965).Twenty egrees C is not ethal o eggsof ome temperate pecies(Sergeev 940). Hypothesis b) is very eneral ecause t argues n advantage or ggretention henever he ground s cooler than the mother nd the young benefit yearlier hatching. Early hatching could be advantageous for various reasons inseasonal environments, uch as seasonal food availability r the approach of winter(Packard et al. 1977).Such generality might imit heusefulness f the cold climatehypothesis b) were t not for qualification. he cost of retaining ggs s likely o beproportional o the duration of retention, hereas he benefit epends upon howmuch the offspring's evelopment s accelerated.A long duration f retention illhave little ffect n development ime f the ground s only slightly ooler than themother. hus, environments hich re cold by other tandards harmful o embry-ogenesis) re the ones likely o provide he most benefit rom gg retention.

There s one critical est f he bove cold-climate ypotheses hatmaybe feasible.Hypotheses a) and (b) cannot explain egg retention n a female hat ays several

clutches er season, unless t s only the first nd/or astclutch hat sretained. f eggretention s found n such a female, hen here s likely nonthermoregulatory asisfor ts evolution.

The strong orrelation etween old climate nd origin f ive-bearing oes notindicate hat we have anticipated hecorrect eason for he orrelation. lthough weand others ave suggested hat old climate sthe volutionary auseof ive-bearing,it could be that old climatemerely orrelates with ome other actor hat s a moredirect ause of ive-bearing r that old climate s indeed he cause but that we havemisinterpreted ow it selects for ive-bearing. or example, Tinkle and Gibbons(1977) suggest hat he volution f ive-bearing n coldenvironments aynot haveathermoregulatory asis. Instead they uggest hat cold climates i) are variable, othat eggs n a nest face many unpredictable ourcesof mortality, nd (ii) lengthendevelopment, hus exposing the eggs to even more sources of mortality hanotherwise. n the Tinkle nd Gibbonsmodel, etention volves o shorten he ntervalin the nest, not necessarily oshorten he total ncubation ime. urther lucidationof hese lternative ypotheses equires etailed tudies n specieswith ggretention,but at present here s circumstantial vidence n favor of the thermoregulatoryhypothesis b)for hree pecies, acerta muralis, . viridis Cooper 1965), nd Natrixnatrix Smith 1973).All three peciesshow the ntermediate tages of egg retention

and all inhabit environments o cold that there s insufficient ime to permitspring-laid ggs to hatch before winter. Natrix natrix not only shows lengthy ggretention, ut also nests in compost heaps, the warmest vailable microhabitat.Despite this, ggs do not hatch beforewinter f the summer s cold (Smith 1973).



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SUMMARY

Most reptiles ay eggs, but many izards' nd snakes give birth o liveyoung byretaining he ggs within he oviducts ntil irth. he origin f ive-bearing n reptiles

is investigated ere by posing a theoretical model and testing he model withpublished ata. Predictions re (1) that ive-bearing hould evolve n cold environ-ments nd (2) that maternal are of the eggsfacilitates heevolution f ive-bearing.Analyses f data from ver 1,000 pecies f izards nd snakes reveal hat ive-bearinghas evolved recently t least 38 times, and an additional 60 species show theintermediate volutionary tages (egg retention). ests of these data support thepredictions: pecies which have recently volved live-bearing r show the inter-mediate tages re much more ikely o be found n cold climates r have maternalcare of ggs han re squamates n general. he presentation n this paper differs romthose of most earlierworkers n distinguishing hecases in which ive-bearing risesfrom hecases in which live-bearing pecies radiates nd invadesnew habitats.

ACKNOWLEDGMENTS

We dedicate this paper to Henry S. Fitch (University f Kansas). Without hispioneering work on reptilian ife histories, nd particularly is 1970 review ofsquamate reproduction, hepresent tudy would not have been feasible.

Raissa L. Berg University f Wisconsin)kindly ranslated he paper by Sergeev(1940)from Russian to English.We thank Donald W. Tinkle for encouragement,

useful suggestions n an earlier manuscript, nd for a copy of an unpublishedmanuscript. We are also grateful o H. S. Fitch, 0. Cuellar, E. L. Charnov, G. H.Pyke, J. M. Legler,G. C. Packard, S. N. Salthe,A. E. Greer, nd J. H. Werren ortheir omments.We gratefully cknowledge he support of a University f UtahPosdoctoral Fellowship to RS) and a University f Utah ResearchFellowship toJB). We thank Toni Kinser for yping hemanuscript.

APPENDIXTHE EVOLUTION OF EGG RETENTION

It is useful o consider modelwhich ncorporateshangesn fecunditynd survival ounderstand ow election ctson the volution f ggretention. ince his aper ealswithreptiles, he model ncorporates ssumptions hich pproximate he natural istory freptiles: verlappingenerations ith eproductiont regular ntervals. achreproductionslimited o one clutch f eggs, nd we further ssume hat dult urvival nd fecundity reindependentf ge. Theaverage ecundity f female n uch populationanbe representedby he eries

sbRo = sb + spb + sp2b+=+ (A1)

in which is uvenileurvival romaying ofirst eproduction, sfecundityndaughters,ndp is adult urvival rom ne reproductionothe next e.g.,Wilson nd Bossert 971).n apopulationonstantnnumber, ecundityRo) sa measure f itness,nd t canbe shown hata rare ominant enewhich ncreases oin femaleshaving oeffect n sex ratio r malefertility) ill ncrease n frequencytechniquen Charnov 979). hus,wehave he ntuitiveresult hat electionn a stable opulation avors genewhich ncreases ecundity. n the



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notation f Al), fecundity ncreases fs'b' sb

> or

b' i-p'S'b > s (A2)

with primes ndicating he parameters f the rare type.Result A2)is at least qualitatively pplicable to the evolution f egg retention. n the text

we suggest hat the general ffect f egg retention s to lower fecundity nd adult survival.Thus, we often xpect b'/b 1 < (1 - p')/(l - p). Under these conditions, gg retention smost likely to evolve if egg survival s' is much greater than s. If however, b'/b,(1 - p')/(l - p) - 1, then s need not increase greatly, nd egg retention s again likely oevolve.We look for he ecological conditions ending oward ither xtreme f ' > s or b'lb,(1 - p'A/l - p) - 1.

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