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P< Ri: R AE D O Ct-M Q< U o o -l0) P< o -f Lf rQ <-- ri: r 0'' aq d < l-\ T] U! AE tJ o UJ6 o ct-m xs tT I +.^ )- Q< 6H'n x'r' sin O -' .u,J O rn :_UJ 0-'q o! Qm7 m m ll >H ;#[r =io f o 0)- A-ds 6 f o (! a EE-II 0 CctNTENTEi €jc,7 I. INTFIOEtUCTIclN 607 II. TEFIMINOLctGtY VIVIPAFIITY 60E| III. HYPOTHE€tEg] ctN FTEPTILIAN A. TyPes of HyPolrheses' 608 Factons' 603 B. Hypotheses Based on Envinonrnent'al 61O C. Hypotheses Eased on Species Chanacl'enisl'ics' 13 ctF HYPOTHESES €i IV. AEiSUM]'TION€I ANEI LctGTC A. Genenal, 613 613 B. Ovipanity as the Pnimitive Condition' C. The Cos1, of ViviPanitY' 6'1 4 615 D. The lrnpontance of Intenmediate Stages' 6'1 6 E. Causes of Egg Montality in the Wild' F. Thenmal Felations of Eggs' 617 G. The Fole of Unpnedictabilitv' 618 HYPCTTHEE;EA 619 V. EMPIFTICAL SUPPGIFTT FOFI THE A. Genenal, 5'1 g B. The Cold-Climate Hypol;hesis' 619 Hypothesis' 62''l C. The Envinonmental UnpnedicEability D. Othen Envinonrnental Factons' 621 E. Defensive AbilitY' 622 F. Othen Specres Chanactenistlcs' 623 G. Ovenview, 624 \/IVIPAFTITY IN VI. EVGILUTIGINAFTY ctFIIGINEi ctF Ei25 ETOUAMATE FIEPTILE€i A. Genenal, 625 B. AmPhisbaenia, 625 C. Saunia' 626 tr}. SenPentes, 645 66c, VII. EVALUATIGIN CtF CASE HTEiTclFIIE€i 660 A. Fnequency of Evolution of Vivipanity' E}. Taxonomic Biases, 663 C. Evaluation of HYPotheses' 665 677 vilr. coNcLuEtloNEt Eiao ACKNC'vt,LEEtGIMENTCI 6E'l FTEFEFIENCEEi TEFIMINOLclGY I. INTFIc'ElUCTIclN (turtles €j07 Of the four orders of living reptiles, three are entirely oviparous and crocodilians),but approximately one-fifth of all speciesof lizards, 6c,7 snakesand amphisbaeniansare viviparous. Most egg-laying squamates 604 studiedto dateretain eggs in uterofor almostone-half of the totalperiod of embryonic developmentand, thus, have evolved part of the way toward viviparity (shine, 1983a).Clearly, viviparity has arisenmany times (e.g., 60s Tinkle and Gibbons, 7977;Shine and BuLl, 7979),and the dichotomy be- : Al fl tween oviparity and viviparity is a puzzling aspectof reptilian reproduc- 613 tion. Consequently,it has attractedconsiderable attention. (For recent re- views seePackard et al., \977; Tinkle and Gibbons,7977; Shine and Berry, 1978;Shine and Bull, 7979;Pllorge and Barbault,1981; Blackburn, 7982') severalhypotheses have been proposedto explainwhy live-bearinghas evolved;most of theseinvoke factorsthat kill eggs in the nest, but not irl utero,andhence favor the evolution of prolongeduterine retentionof eggs. Theory also suggeststhat certaintypes of speciesshould be most likely to evolve viviparity; specifically,groups in which the survivorship or food intake of the reproducing female would not be markedly affectedif she 619 retained eggsii utero.The present review examinesthe validity of these ideas in tJrms of the arguments and inherent assumptionsin each hy- pothesis,summarizes the empiricalsupport for eachhypothesis (based on publishedliterature), and testspredictions from thesehypotheses by iden- iiryir,g the squamatelineages in which viviparity has evolved-andby look- ing for the ecologicalcorrelates predicted by theory. For this purpose/ u'u"uilubl"phylogenetic and reproductive data on taxa containing both oviparous and viviparous forms are reviewed. II. TEFIMINClLG,G;Y Most reptilesreproduce by laying shelledeggs that containrelatively unde- veloped embryos;they are termed oaiparousor egglaying.However, many squamatespecies retain eggsin uterountil embryonicdevelopment is com- pl"tu. tn these casesthe young are fully formed at birth and are capableof independent movement and feeding; this reproductive mode is referred to as liae-bearingor oiaiparitY. Some authors have restricted the term viviparity to species with an intimate physiological connectionbetween the reproducing female and her 677 uterine ybttttg; this may involve complex placentation, absenceof calcified ciao egg-membrar,es,o. maternal-fetaltransfer of nutrients (Weekes, 1935; Bauchot, 1965;Spellerberg, 1976). Although the distinction between ooo- 6Cl1 aiaiparity (no maiernal-fetal nutrient transfer) and euaiaiparitymay be at- tractiveionceptually, it is difficult to apply to reptiles. The availabledata Eiog THE EVGILUTIG'N OF \/IVIF'AFIITY IN suggest that most, but not all, live-bearing reptiles are ovoviviparous (Thompson,7987; Yaron, Chapter 7, this volume). Exceptionsto this state- ment include the New World skinks of the genus Mabuya, n'hich show reduced ovum size and extensivematernal-fetal nutrient transfer (Vitt and Blackburn, 1983). Throughout this chapter, I use the term oaiparitrlin those cases where shelled eggs are laid, and uiaiparity where yourlg are either born alive or are deposited in thin-walled membranous sacs from which they emerge within a few days of parturition. This terminology follon's the recommendations of Smith et al. (1973), Guillette (1982a), and Yaron (Chapter 7, this volume) and corresponds to that used by most authors (e.g., Weekes, 1933; Rahn, 1939; Dumas, 1964; Neill, 1964; Greer, 1966; jenkins and Simkiss , 7968; Greene, 1970; Yaron , 7972; Huey, 1977; Sexton and Claypool, 1978; Thompson, 7987, 7982). III. HYPGITHESEsi clN FIEPTILIAN VIVIPAFIITY A. Types of Hypotheees The selectiveforces underlying the transition from oviparity to viviparity have been a subject of speculationfor many years. The resulting hypoth- "benefits" "costs" esesmay be framed in terms of the relative and of the two reproductive modes to a female reptile, that is, the probablelifetime production of offspring (: fitness)of an oviparous femaleis comparedto that of a viviparous femaleunder a variety of parallelecological conditions. Most authors have emphasizedthe benefits of viviparity in terms of an increasein the number of surviving offspring (e.9., Weekes,1933; Neill, 1964).Eggs retained in uteromay be protectedfrom many sourcesof mor- tality, which they would normally experiencein the nest: for example, extremesof temperature or humidity, fungal attack, and predation. The benefit from viviparity could equally well be the loss of a cost associated with oviparity: for example, the need for reproductive femalesto make long and possiblyhazardous journeys to suitablenesting areas (e.g., Neill, 1964;Fihch, 7970). However, it is misleadingto look only at the benefitsof viviparity and to ignore the associatedcosts. A more balancedview considersthat viviparity may increasethe fitness of a femaleonly under a limited set of condifions (e.g., Fitch, 1970;Tinkle and Gibbons, 7977;Shine and 8u11,1979). Al- though viviparity may benefit survivorship of the offspring, it also may confer a cost to the food intake of the reproducing female,to the probabil- ity of her survival, and to subsequentfecundity. The nature of thesecosts can be used to frame predictions about the types of speciesor habitats in which viviparity would be most likely to evolve (Fitch, 1970;Shine and Bull,7979). In summary, both viviparity and oviparity confer costsand benefits.The HYPGITHESES clN FTEPTILIAN VIVITAFIITY ; are ovoviviparous advantages of viviparity may lie primarily lvith increasing survivorship of eptions to this state- the offspring, whereas its disadvantages may lie with the effects of physi- labuya,which show cally burdening the female with eggs for a prolonged period. The relative rnt transfer(Vitt and importance of these advantagesand disadvantageswill depend upon both rm ouiparityin those environmental conditions and speciescharacteristics. published hypoth- rre young are either esesregarding possible selectiveforces are revierved belorv. ,us sacsfrom which rinology follows the B. Hypotheses Elased on Environm€ntal Factors (1982a),and Yaron ed by most authors 1. COLD CLIMATES ,7964; Greer,7966; The earliest and the most widely accepted hypothesis of reptilian viviparity Huey, 7977;Sexton is that it evolved as an adaptation to cold climates. Tinkle and Gi6bons (7977)traced this idea to Mell (7929) and cite several examples that indicate its currently widespread acceptance. The argument usually runs as fol- lows. In cold climates, behavioral thermoregulation allows the body tem- VIPAFIITY perature of females to be much higher than that of the soil. Thus, eggs retained in utero will develop at higher temperatures (and hence more rapidly) than will eggs deposited in the soil. Early hatching, due to ac- celerated development, may be adaptive in at least the three following iparity to viviparity ways: (1) Eggs may hatch prior to the onset of lethal autumn frosts. (2) e resulting hypoth- ' "costs" Eggs spend less time in the soil in which they may be vulnerabre to factors and of the such as predation and desiccation. (3) Early hatching enables the offspring te probablelifetime to feed and accumulate energy reserves before hibernation, thus increising nale is comparedto their chances of survival over winter and subsequent growth rates. "cold-climate" ologicalconditions. An alternative and simpler version of the hypothesis is :rity in terms of an that soil temperatures at the time of ovulation will be y'eekes, so low as to be lethal 1933;Neill, to developing eggs. Thus, unless body temperatures of gravid females falr rny sourcesof mor- to soil temperatures, uterine retention will protect eggs from these lethal nest: for example, extremes (Shine and Bull, 7979). (The same argument can be applied to rnd predation. The very hot climates in which uterine retention might protect eggs from le- rf a cost associated thally high temperatures; Shine 'e and Bull, 1979). Also, high elevations may females to make play a role in stimulating the evolution of placentation, because
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