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"" " The American Naturalist Vo\.I13,No.6 THE EVOLUTION OF LIVE-BEARING LIZARDS AND SNAKES June 1979 IN RICHARD SHINE. AND J. J. BULL Department of Biology, University of Utah, Salt Lake City, Utah 84112 Most reptiles lay eggs, but many lizards and snakes are live-bearers. Taxonomic and embryological evidence indicates that egg-laying is ancestral (Weekes 1935; Matthews 1955; Amoroso 1960), so the common occurrence of genera containing both live-bearers and egg-layers shows that live-bearing has arisen from egg-laying several times (table 1). This paper considers the ecological conditions favoring the evolution of live-bearing in squamate reptiles. There have been several excellent treatments of reptilian live-bearing which have made this current synthesis possible (Melll929, Weekes 1935; Sergeev 1940; NeillI964, 1971; Packard 1966; Greer 1968; Fitch 1970; Greene 1970; Packard et a\. 1977; Tinkle and Gibbons 1977). Here a comprehensive model is presented to account for the evolutionary origin of livebearing, and published data are used to test predictions from the mode\. ORIGIN VERSUS MAINTENANCE The evolution of live-bearing from egg-laying in squamate reptiles is almost certainly a grad ual process. In the early stages of this process, females carry the eggs long enough to permit some embryonic development in utero but lay the eggs prior to the completion of embryogenesis. Continued selection for progressively longer egg retention eventually results in complete intrauterine incubation (live-bearing). Certain physiological and anatomical changes must accompany the transition from egg-laying to live-bearing (Weekes 1935; Bauchot 1965; Yaron 1972). These requirements probably prevent any rapid evolutionary "jump" from egg-laying (without in utero development) to live-bearing. For example, the female must develop vascular structures for gaseous exchange between oviducts and offspring, and she must maintain only a thin egg shell around them while they are in utero. These modifications must be l1ore extensively developed in females that retain eggs a long time than in females tLat retain eggs only a short time, because the need for exchange between mother and offspring increases as the embryos become larger (DmieI1970). Thus, even females capable of retaining eggs for short intervals are not necessarily capable of sustaining eggs in utero throughout development. Packard et a\. (1977) also provide supporting evidence for these assumptions. In order for live-bearing to arise from egg-laying, selection must favor the intermediate stages in which females retain eggs for progressively longer periods of * Present address: ZoQlogy Department, University of Sydney, New South Wales 2006, Australia. Am. Nat. 1979. Vol. 113. pp. 905-923. ,1') 1979 by The University of Chicago. 0003-0147(79/1306-0009$01.65 906 THE AMERICAN NATURALIST time. There may be circumstances in which it is advantageous to be live-bearing, but in which the intermediate stages of egg retention are not favored (Weekes 1935; Tinkle 1967; Packard et al. 1977; Tinkle and Gibbons 1977). A major difference between a live-bearing female and an intermediate egg-retaining female is that the live-bearer is emancipated from nesting while the intermediate female is not. If the act of nesting is strenuous or risky, then an advantage accrues to live-bearing but not to the intermediate stages of egg retention. In discussing the evolution of live-bearing it is therefore necessary to distinguish forces which provide an advantage for these intermediate stages (i.e., favoring the origin) from forces which merely provide an advantage for the maintenance of live-bearing. This paper investigates only the origin of live-bearing. The maintenance of live-bearing is considered by Sergeev (1940), Tinkle and Gibbons (1977), and Shine and Berry (1978). ECOLOGY How will selection act upon a female carrying her eggs slightly longer than the average female, thus allowing the young to develop in utero and spend less time in the nest? The fitness parameters most likely to be affected by oviducal retention are (1) offspring survival, an~ (2) mother survival and future fecundity. Egg retention is most likely to be favored when either (i) the survival of young is greatly improved by oviducal retention, or (ii) the mother does not lower her future fecundity if she carries the eggs longer (Appendix). Some ecological factors which may favor egg retention in the;:seways are discussed below. Also, we attempt to distinguish factors which can select for the complete evolution of live-bearing from factors which select only for short intervals ?f egg retention. Factors Affecting Egg Survival 1. Temperature.-Proper embryonic development in squamate reptiles requires a limited range of temperatures, and temperature extremes may be fatal (Fitch 1964; Licht and Moberly 1965; Vinegar 1974). Also, the rate of embryonic development is proportional to temperature in some species (Blanchard and Blanchard 1941; Fitch 1954; Platt 1969). The fitness of hatchlings therefore depends upon incubation temperature to the extent that embryogenesis must be normal and hatching occurs during some optimal time. Certainly the mother should lay eggs in the sites which are most thermally suitable for development, but some environments may be so extreme that ideal nest sites are not available and eggs will inevitably be exposed to non optimal temperatures. Such thermal unsuitability may be, characteristic of cold environments and possibly of hot environments. Cold environments may adversely affect the fitness of hatchlings for the two reasons outlined above: (a) The nest substrate may be cold enough to harm embryos, and (b) the cold nest may slow development so that hatching occurs later than some optimal time. These two effects are not necessarily independent, but the distinction is useful. As an example of (a), eggs might be laid early enough in the spring to be subjected to late frosts. For (b), montane and some temperate environments could be too cool to permit spring-laid eggs to hatch sufficiently long before winter. EVOLUTION OF LIVE-BEARING 907 Cold environments are unique in that short intervals of egg retention may overcome athermal complications during development. In the example of (a), egg retention would avoid exposure of eggs to the frosts, since the mother could seek shelter at frost-free depths. In the example of (b), egg retention would lead to early hatching if the mother maintained a body temperature higher than substrate temperature during part of the day. When laid, embryos would be developed further than if they had remained in the ground during the same interval. It is in fact known that females of some species accelerate development by thermoregulating when they retain eggs, and thus hasten hatching (Sergeev 1940; Blanchard and Blanchard 1941; Stewart 1965; Hirth and King 1969; Osgood 1970; Packard et al. 1977). Cold environments need not always favor egg retention, though. The time of hatching cannot be hastened if the development Tate is temperature-independent (e.g., Chelydra, Yntema 1968) or if the mother maintains the same temperature as the substrate (aquatic or fossorial species, Brattstrom 1965). Cold environments should therefore often select for egg retention, as suggested previously (Mell 1929; Weekes 1935; Sergeev 1940; Packard 1966; Greer 1966; Packard et al. 1977). In addition, cold environments favor the progressive evolution to live-bearing because they often occur as gradients from warm to cold habitats, with latitude or altitude. As populations of individuals that retain eggs become established in cool areas, selection can favor increased retention times among the invaders of even cooler areas. This can progress until live-bearing evolves. Temperature extremes are less likely to be a problem in hot environments than in cold environments, because hot environments usually contain many microhabitats that do not experience harmfully high temperatures. It is conceivable, though, that egg retention could.~volve in response to rapid seasonal changes in ground temperature, as in some deserts. A shallow nest sufficiently warm in spring may become too warm later, before hatching. A deep nest may never become too warm, but could lead to late hatching because it is too cool in spring. Some benefit may be derived from retaining eggs until the environment passes through the temperature fluctuation. This does not seem as compelling a cause for the evolution of egg retention or livebearing as cold environments, however. 2. Predation.-Predation is a source of high egg mortality in many reptiles and therefore may lead to selection for egg retention. The benefit of retaining eggs depends upon how predation is reduced by late laying and less time in the nest. Conceivably, egg retention could evolve in response to predation when the risk of predation is proportional te' the time spent in the nest. However, available data indicate that predation is n\ t proportional to the time of incubation. In the cases studied, predation has proven to be high just after the eggs have been laid, and possibly high when the young emerge, but predation may be slight in between (Blair 1960; Moll and Legler 1971; Carr 1973). Egg retention will reduce predation only slightly under these circumstances, because its only effect is to shorten the interval in which there is little mortality. With this form of predation live-bearing will be favored over egg-laying, but the intermediate stages of egg retention probably confer no advantage. 3. Moisture extremes.-Some authors have proposed that the two extremes of moisture content in the nest (wet and dry) select for live-bearing (Weekes 1935; Neill 908 THE AMERICAN NATURALIST 1964). Neill proposed that eggs laid in wet soil are subject to infection and that this selects for live-bearing. Other possible reasons for mortality in wet or dry nests are conceivable. Unfortunately, no meaningful discussion of these factors is yet possible because little is known about egg mortality in wet or dry nests. It is also difficult to draw correlations between egg retention and nest humidity because information is lacking on the nesting sites of most species. A species that occupies a wet habitat may be able to locate dry nesting areas, and vice versa. Even if wet or dry soil lowers egg survival, retention need not be favored. Retention should evolve only if the mortality falls chiefly on the early stages of embryogenesis, or on eggs that remain in the nest slightly too long. Otherwise a reduction in time spent in the nest will not greatly increase egg survival. There is one case in which short intervals of egg retention may evolve because of nesting in dry habitats. If a long dry season preceeds egg laying and rain usually comes at the onset of nesting, then it may be advantageous to delay laying until it rains (Gehlbach 1965). Eggs are thus laid in moist soil, possibly increasing their survival. Egg retention per se need not offer an advantage to the eggs, but if the timing of the rain is unpredictable and the mother must lay sQon after precipitation, then early ovulation allows her the flexibility of laying at any subsequent time (Steams' "bet hedging," [1976]). Of the ecological factors which affect egg survival, a cold environment is the most appealing cause for the evolution oflive-bearing. Although there are many sources of egg mortality which may be improved slightly by retention, cold environments are unique in that (i) they can be lethal to embryos, (ii) they can be compensated for by short increases in retention time, and (iii) they occur in graded elines, allowing progressive evolution to live-bearing. Mortality sources which are proportional to the time spent in the nest do not have as high a benefit/cost ratio for egg retention. Factors Affecting the M other A female laden with eggs is less efficient at locomotion and, hence, may be more vulnerable to predators and less able to forage than if she had laid the eggs (Fitch 1970; Tryon and Hulsey 1976). Egg retention is perhaps most disadvantageous to mothers of species in which females move about actively after laying eggs. If the female did not retain eggs, she could be moving about and feeding sooner. However, there are many species in which the female coils around the eggs and stays with them throughout incubation. These "brooding" females usually do not feed during this time (FitzSimons 1919; Pope 1935; Fitch 1954; Sweeney 1961; T.aylor 1965; Leakey 1969). Retention may not be costly to such a female, because it does not prolong the interval in which she abstains from feeding. 1. No maternalcare after laying.-Perhaps the main cost of retaining eggs is the mother's decreased mobility. This makes her less able to feed and more vulnerable to predation. Egg retention should be least disadvantageous in species that are least prone to predation or that do not depend on rapid movements for feeding. Livebearing should evolve most often in species that are (1) large and deadly, because they can ward off predators (Mell 1929; Sergeev 1940; Neill 1964); (2) secretive, EVOLUTION OF LIVE-BEARING 909 because they rarely encounter predators (Melll929; Fitch 1970); or (3) slow moving, because they do not depend on speed to escape predators or to catch food (Fitch 1970). In contrast, arboreal species which rely on agility to feed or to avoid predators should be at a greater disadvantage when retaining eggs. The above comparisons assume that females continue to move about and feed while retaining eggs. This is only likely to be true for short intervals of retention. Females of many snake and lizard species become very secretive and curtail their activities when carrying eggs for a long period, even in large and deadly species (e.g., the live-bearing snakes Vipera, Prestt 1971; Crotalus, Keenlyne 1972; Sistrurus, Keenlyne and Beer 1973; Agkistrodon, Fitch and Shirer 1971; Notechis, Pseudechis, Shine 1978). This tends to equate the cost of egg retention among the different specIes. Retention might evolve because of short-term events that affect the ease and safety of nesting. For species that dig or construct nests (mainly lizards), rain may facilitate the construction of a nest in a dry area. If nesting occurs at the time of year when rains begin, then the female may be favored to retain eggs until rain falls (Anderson 1962). (Recall that egg survival may also be enhanced in this situation.) Long intervals of retention need not be favored since the advantage of waiting may be outweighed by the disadvantages of long-term retention. 2. Maternal care.-Egg retention may not be as costly to a mother if she broods the eggs from laying until hatching: By carrying the eggs longer, she does not have to brood them as long. This compensation means that egg retention is tnore likely to evolve in a brooding species than in a nonbrooding species. Brooding may even favor egg retention, but may not suffice to favor live-bearing. During the early stages of developmcnt.,retention may be less costly than brooding, because retention allows the mother freedom of movement to feed. As the embryos develop, the eggs increase in volume and weight, and the mother becomes more heavily burdened (e.g., Fitch 1954; Shine 1977). Eventually, it becomes advantageous to cease moving around and to lay the eggs. Cold environments provide an advantage for retention in a brooding species that does not apply to a non brooding species. In cold environments the mother's high body temperatures can accelerate embryonic development during retention. This shortens the total incubation period (retention plus brooding) and therefore may decrease the mother's total interval of parental care. Live-bearing may therefore evolve from brooding in cold environments even if egg survival is not affected. 3. Other previous hypotheses.-i) Prolonged egg retention delays the time at which the mother can ovulate ller next clutch. This might be a major disadvantage in species that lay more than one clutch per season (Sergeev 1940; Tinkle and Gibbons 1977) ii) Two common arguments in the literature are that live-bearing evolves in aquatic or arboreal species because the mother is freed from having to leave her usual habitat in order to find a suitable nesting site (Melll929; Sergeev 1940; NeillI964; Fitch 1970). Clearly, this does not apply to the intermediate stages (because the mother still has to find a nest), and therefore will not lead to the evolution of live-bearing (Packard et al. 1977). The arboreal habit may even select against the evolution of live-bearing (see above). 910 THE AMERICAN NATURALIST PREDICTIONS The preceding discussion yields three predictions to be tested. I. Egg retention and live-bearing should evolve in cold climates, because egg retention may confer advantages in avoiding lethal temperatures and in hastening the time of hatching. 2. Egg retention and live-bearing should evolve more readily in species with female parental care than in species without female parental care, because the costs of egg retention to the mother are little, if at all, higher than the costs she already faces in brooding. 3. Egg retention and live-bearing should not evolve as a response to aquatic or arboreal life. or extremes of soil moisture, because intermediate stages of egg retention are not favored. Two other predictions are not tested here. 4. Egg retention may evolve most readily in large, deadly species and in secretive species, because the mother is not vulnerable to predators. A problem in testing this prediction is that ]arge deadly species and secretive species are likely groups to show brooding behavior, which in itself is likely to favor egg retention. 5. Egg retention may evolve more readily in single-clutching species than in species which produce more than one clutch per year, because egg retention does not interfere with the mother's immediate future fecundity in single-clutching species. This hypothesis is not tested because the data for clutch frequencies are not available for populations showing egg retention. This test also requires separating the effect of cold and brooding from single-clutching, because these factors will often be correlated (Fitch 1970). TEST OF PREDICTIONS The live-bearing habit may be favored over egg-laying under many conditions that do 110tfavor the origin of live-bearing. Thus, the habitats occupied by live-bearing species may often be different from the habitats in which live-bearing evolved. To test the predictions, we must isolate the cases where live-bearing is evolving or has evolved recently from cases in which live-bearing has a remote ancestry. This can be done by considering the following two categories of data, also recognized by Sergeev (1940). i) Recent origins qf live-bearing.--Live-bearers and egg-layers co-occur within some genera, within some subgenera or species groups, and even within some species (table]). This indicates that there has been a transition from egg-laying to livebearing (or the reverse) subsequent to the common ancestry of these populations. The transition from egg-laying to live-bearing is more likely than the reverse (Fitch 1970: Tinkle and Gibbons 1977), so we infer that these cases.represent origins of live-bearing. The fact that these origins are recent (by virtue of limiting the data to origins within a genus or smaller taxon) suggests that the ecologies of these live-bearers may still represent the environments which favored the evolution of live-bearing. Where live-bearers and egg-layers co-occur at higher taxonomic levels, this supposition is not likely to be true. EVOLUTION 911 OF LIVE-BEARING TABLE 1 RECENT ORIGINS OF LIVE-BEARING. Proportion of Live-Bearing Species In Cold Climat<::s Family, Genus Lizards Chameleontidae Chamaeleo ........... 3/3 Iguanidae Corytophanes . . . . . . . . . Lio/aemus............ Phrynosoma ... . . . See/oporus aeneus S. formosus group S. sea/oris group. ..... S. variahilis group. . . . . Scincidae Anoma/opus ... Eumeees............. Lei%pisma (New Zealand) (Tasmania) ..... Anguidae Dip/og/ossus GerrllOnot!ls McCoy 1968 Donoso-Barros 1966 Stebbins 1954; Lowe and Howard 1975 1/1 2/2 1/1 1/1 Davis & Dixon Stuart 1948; Fitch 1970; Werler 1951 1/1 A. E. Greer, personal communication Axtell 1960; Van Devender and Van Devender 1975; Webb 1968; Legler & Webb 1960 Barwick 1959; Cogger 1975; Rawlinson 1976; McCann 1955 Loveridge 1942 Greer & Parker 1967 Greer 1977 Horton 1973 Smith 1935; Horton 1973 Smith 1935 + 15/15 5/5 ?/I 1/1 0/4 7/10 1/1 1/1 2/3 1961; ?/1 Greer & Parker 1974; Fitch 1970 Greer & Parker 1968 2/2 1/1 Sergeev 1940 Smith 1973 .... 2/4 + .......... 9/9 + Agamidae Phrynoeepha/us Authority Schmidt & Inger 1957 1/1 13/20 3/3 3/3 Leptosial'hos ..... Lerista .......... Lygosoma........ Mabuya (South Africa). Mabuya (Asia) ....... Scinee/la............. Sphenomorphus (New Guinea) . . . . . . Tribilonotus . . . Lacertidae Eremias ............ Laeerta.............. Maternal Care Known in Taxon? 1/1 Greer 1967; Taylor 1956; Lynn & Grant 1940 Stebbins 1958; Greer 1967 Smith 1935; Minton 1966 (Continued) EVOLUTION 911 OF LIVE-BEARING TABLE 1 RECENT ORIGINS Proportion of Live-Bearing Species In Cold Climate:s Family, Genus Lizards Chameleontidae Chamae/eo ...... Iguanidae Corytophanes . . . . . . . . . Lio/aemus . . . . . Phrynosoma See/oporus aeneus S. /ormosus group S. sea/aris group. S. variahilis group. Scincidae Anoma/opus .... .......... Eumeees ............. Leptosiaphos Lensta Maternal Care Known in Taxon? 3/3 McCoy 1968 Donoso-Barros 1966 Stebbins 1954; Lowe and Howard 1975 111 2/2 111 111 Davis & Dixon Stuart 1948; Fitch 1970; Werler 1951 I11 A. E. Greer, personal communication Axtell 1960; Van Devender and Van Devender 1975; Webb 1968; Legler & Webb 1960 Barwick 1959; Cogger 1975; Rawlinson 1976; McCann 1955 Loveridge 1942 Greer & Parker 1967 Greer 1977 Horton 1973 Smith 1935; Horton 1973 Smith 1935 + 15/15 515 .... . Lyyosoma........ Mabuya (South Africa). Mabuya (Asia) .. Seineella............. Authority Schmidt & Inger 1957 111 13/20 3/3 3/3 Lei%pisma (New Zealand) (Tasmania) ........ OF LIVE-BEAkING* ?/I 111 0/4 7/10 I11 I11 1961; SphellOmorphus Tribi/onotus Lacertidae Eremias ............. Laeerla.............. Anguidae Dip/og/ossus . . . ?/l Greer & Parker 1974; Fitch 1970 Greer & Parker 1968 2/2 111 Sergeev 1940 Smith 1973 2/3 (New Guinea) ... 2/4 + GerrllOnotus 9/9 + Agamidae Phrynoeepha/us 111 Greer 1967; Taylor 1956; Lynn & Grant 1940 Stebbins 1958; Greer 1967 Smith 1935; Minton 1966 (Continued) 912 THE AMERICAN NATURALIST TABLE I (Continued) Family, Genus Proportion of Live-Bearing Species In Cold Climates Maternal Care Known in Taxon? ?/I + Authority Snakes Typhlopidae Typhlops Colubridae ...... Aparallactlls . .. Coronella ............ Elaplre . .............. Helicops. . Oplteodrys vernalis Sinol1atrix ........... Viperidae Cerastes Echis Vipera Crotalidae ........ . + ?/I 1/1 1/1 + ?/I 1/1 2/4 + ..... 2/4 + .' 1/1 AgkistrodOI1 (Asia) .... 1940; Taylor 1965 Pitman 1974 Smith 1973; Street 1973 Pope 1935; Oliver 1959; Fukada 1965 Rossman 1973 Ditmars 1942 Pope 1935; Smith 1973 Domergue 1959 Minton 1966; Mendelssohn 1965; Duff-Mackay 1965 Mendelssohn 1963 3/5 .............. Trimeresurus 0/1 1/1 1/1 Bogert Pope 1935, Smith 1943: Wall 1921 Pope 1935: Fukada 1964: Nickerson 1974 Elapidae Pseudechis . Covacevich personal & Tanner, communication NoTE.-Symbols: + = yes: - = no; ? = insufficientdata. Genera. species groups, or species containing populations of egg-layers and live-bearers (taking the smallest taxon containing both types) with data on habitat. climate, and maternal care in the taxon. We have omitted doubtful records (Tinkle and Gibbons 1977; Spellerberg 1976; Packard et al. 1977), and cases where continents have been colonized by live-bearers. ii) lntermediate stages of live-bearing.-Many species retain eggs long enough for embryonic development to reach a visible state at the time of laying (table 2). These species have progressed part of the way toward evolving live-bearing and should therefore indicate the ecological factors favoring the evolution of live-bearing. In order to test the hypotheses, we assembled ecological data from published literature for live-bearers with congeneric egg-layers and for species with egg retention (tables 1, 2). In addition, we gathered the same ecological data for over t ,000 species which show neither live-bearing nor egg retention (table 3). These latter data serve as an estimate of the "expected frequencies" of the various ecologies for squamates as a whole; they form the basis for testing for a bias in the ecologies of the live-bearers and egg-retaining species. The assignment of these species to the different ecological categories was based on ecological descriptions in the sources (table 3, footnote). In the absence of absolute definitions of cold climate, wet or dry habitat, and so forth, a relative measure was used for these ecological categories in each continental area. This no doubt introduces subjectivity into these assignments, but no alternatives seem possible at present. Since the tests of significance are themselves EVOLUTION 913 OF LIVE-BEARING TABLE 2 INTERMEDIATE STAGES OF LIVE-BEARING. SQUAMATE SPECIES WITH EGG DATA ON HABITAT. CLIMATE, AND MATERNAL Population In Cold Climate? Family, Species RETENTION; CARE IN THE SPECIES Maternal Care? Authority Lizards Iguanidae Ana/is aeneus A.cybotes ........... 4.shrerei ........... Lialaemus montieola Sceloparus darki S. orclltti . S. sealaris .. S.lIndlllalUs ............ S.rirgatus ........."... Scincidae .4,wtismaeeoyi.......... ElIl/leees brevi/ineatus. ... E. callieephalus. + + + ........ E./aseiatus. ..,......... Leiolopisma guiehenoti L.suteri ........... L.trililleata ........ r'vforetllia boulenge;; Scillcella laterale SaipllOs eqllalis Lacertidae Locerta agilis L. 1/1lira lis . L. I'iridis .. Anguidae Diploglossus delasagra ... Gerrhonotus mlllticarinatlls Helodermatidae Heloderma suspectlll/l Agamidae Calotes I'ersicolor Snakes Boidae Pyt/ll)// molurus Stamps 1976 Huey 1977 Huey" 1977 Donoso-Barros 1966 Kauffeld 1943; Stebbins Stebbins 1954; 1958 Anderson 1962 Gehlbach 1965 Vinegar 1975 + + + + + + + + + + + + T.se/llege/;i """""" Colubridae Alwetlllla ahaetul/a ...... Cagle 1940; Fitch Pengilley 1972 Towns 1975 Smith 1973 Cooper 1965 Marshall 1956 + + 1961; 1954 + + + 1967 Greer 1967; Taylor 1956 Stebbins 1954. 1958 Ditmars 1942. doubtful; see Bogert & Dal Campo 1956 + Muthukkaruppan + + + ......... Campbell & Simmons Zweifel 1962 + + .. Pengilley 1972 Werler 1951 Pengilley 1972 Rawlinson 1976 Johnson 1953 Bustard 1965; Cogger P reticulatus P. sebae Typhlopidae Typhlops diardi + 1954 ? + + et al. 1970 Pope 1961; Van Mierop & Barnard 1976 Pope 1961; Fitch 1970 Joshi 1967; Branch & Patterson 1975 Wall 1918; 1921; Smith Taylor 1965 FitzSimons 1962 1943; Smith 1943; Taylor 1956; Pope 1935; Wall 1921 (Continued) 914 THE AMERICAN NATURALIST TABLE 2 (Continued) Population In Cold Climate? Family. Species Amplliesma sto/ata . . . . . . . Ampltiesma rihakuri ..... Aspidl/ra /racltyproc/a . . . . Bnigutrignna/u ......... C urphopltis ["ermis ....... Diadnpllis pl/llc/atus . + + + + + + Eluplle dinne" . . 0. . . . + Eo ohso/eta E. /uellil/ris 0. 0. 0. . . . 0. He/i('(lpsulIgu/a/l/s La/llprore//is triallgull/m LY('(IdcJ/lul//icus Na/rixmallra No /I<I/r;x o.. .. ....... 0..0 0 N. percarilla/a Ol'lteadrys ["erna/is .... f'illlOl'ltis me/(//IO/eI/CIIs. . Psammol'/Irlax rllOmhel/IIIS I'salll/l1op/Jylax /ri/lIelliJlIIs I'rrus dltwlllwdes .. Viperidae Ps"l/doceruste~ + + 00000.0.. 000 E. l'I"pilla Maternal Care? per~!cl/S + + + + + + ? + + + + ? + + + + + Authority WaIl 1921: Minton 1966 Fukada 1956: Malnate 1962 Wall 1921 Wall 1921 Clark 1970 Ditmars 1942: Blanchard 1930; Fitch 1975 Fukada 1965 Ditmars 1942: Fitch 1970 Pope 1935 Zehr 1969 Rossman 1973 Ditmars 1942 WaIl 1921: Smith 1943 Duguy & Saint Girons 1966 Angel 1950; Smith 1973: Parker 1963 Pope 1935 BIanchard 1933; Ditmars 1942: Stille 1954; Minton 1972 Anderson 1965: Car11944 FitzSimons 1962 Sweeney 1961 Pope 1935 + Mendelssohn 1965: Minton 1966 + Pope 1935; Smith 1943; Leakey 1969 Smith 1943 Pope 1935: Wall 1921 Crotalidae Agkis/rodc)/J UClltuS A. rltodosroma Trimeresl/rtls . o. 0 mcm/ico/u Elapidae Cal/inpltis mace/el/andi !If icrl/rtls (I/Irills + + o. + + + + Na;a/lCI;a . Egg retention inferred from short incubation period Soderborg 1973 Ditmars 1942: Mole 1924; Campbell 1973 Pope 1935; Campbell & Quinn 1975 (~ 26 days). merely comparisons of frequencies, subjectivity in the data does not influence the conclusions. provided we have been consistent. 1. Ure-bearillg alld egg retention should evol1"C' ill cold climates:-If cold is a major cause for the origin of live-bearing, then the species or populations which have recently evolved live-bearing should be found in cold climates more often than squamates as a whole. This prediction is supported by the cases in table 1 for which habitat information is available (33 origins). Giving equal weight to each origin (each entry multiplied by the proportion of live-bearers in cold) reveals that 28.1 of 33 cases EVOLUTION 915 OF LIVE-BEARING TABLE 3 DISTRIBUTIONS OF SQUAMATE SPECIES WITH RESPECT TO HABITAT AND OCCURRENCE PROPORTIONS IN EACH CATEGORY All Squamates Cold climate """""""""'" Wet soil. ........................ Dry soil. ........................ Aquatic. . . .............. Arboreal......................... Maternal Live-Bearers in Genera with Both Egg-Laying and Live-Bearing Members (n = 38) ~.14 CARE; Species with Egg Retention (n = 60) .72 .11 .13 .24 .05 .03 .02 .08 .08 .24t .33 care (at generic level) . .44(.13-.61) .12(.04-.22) .18(.03-.35) .05. (0-.14) .10. (.02-.28) OF PARENTAL ................ .lIt Based on data for 1,011 species from Africa, China, Australia, and North America. from Pitman (1914), Pope (1935), Cogger (1915), Conant (1958), and Stebbins (1966); brackets give ranges of the four continental means. Categories were determined by the respective authors' criteria and our personal knowledge of the species and habitats (North America and Australia). t Based on data for 100 egg-laying species (231 genera) in Fitch (1910). t In egg-laying forms. (85'/';,)are found in cold climates. This is significantly different from the proportion in squamates as a whole (44 '\,; Fisher's exact test, P < 10- 5). Even if all of the unknown cases in table I are assumed to inhabit warm environments, the proportion of newly evolved live-bearers in cold climates (28.1of 38, or 74%: tables 1,3) is much higher than among squamates in general (44%; P < .001). Egg retention is also significantly correlated with cold climate: table 2 shows that 43 of the 60 egg-retaining species are found in cold climates, while another 15 (possibly 17) are not. Thus, the proportion of egg-retaining species found in cold climates is significantly higher than that for squamates as a whole (72% versus 44~;"; table 3, Fisher's exact, P < 10-4). 2. Egg retention and live-bearing should evolve more readily in species with female parental care than in species without female care.-Egg retention shows a strong correlation with brooding: 18 of 55 kn )wn brooding species (33 o/~)retain eggs, but only 39 of 650 non brooding species (v,?~) have oviducal retention (Fisher's exact, P < 10-5). In addition, live-bearing has arisen more frequently in brooding than in non brooding genera: Live-bearing has evolved in eight of the IS brooding genera containing more than one species (53 %), but in only 24 of the 150 polytypic nonbrooding genera (16,?~).The difference in proportions is significant (Fisher's exact, P < .005). We must be cautious that brooding species are not disproportionately found in cold environments, as this could account for part of the above correlations, We do not know definitely if brooding is correlated with cold, but the data in table 2 (here) 916 THE AMERICAN NATURALIST and in figure 1 of Tinkle and Gibbons (1977) suggest not. This possible bias can be circumvented, however, by restricting the comparison to taxa in cold climates. Of 13 brooding genera with taxa in cold climates, live-bearing has arisen in 7 of these (54 ~{»),whereas live-bearing has arisen in only 23 %of the non brooding genera found in cold climates (23 of 101 genera; table 3 has only approximations of these data). If we assume that the brooding and nonbrooding genera have had the same number of species in cold climates (equal opportunity for the origin of live-bearing), then the correlation is significant (Fisher's exact, P < .05). Therefore, it seems that brooding enhances the evolution of live-bearing as well as the evolution of egg retention. 3. Egg retention and live-bearing should not evolve in response to aquatic or arboreal life, or to extremes of soil moisture.-If these habitats promoted the evolution of live-bearing, they should contain many species with egg retention and many livebearing species with egg-laying congeners. Table 3 does not support this prediction. Species in these habitats have evolved egg retention and live-bearing about as often as would be expected from their proportions in squamates as a whole (P> .05 in all cases). DISCUSSION Live-bearing has evolved from egg-laying more than 30 times in squamate reptiles. Several hypotheses have been presented here to account for the origin of live-bearing. The model we advocate assumes that live-bearing evolves from egg laying only if the intermediate stages of egg retention are selected for. Egg retention is a state in which females delay laying and carry the eggs to allow partial embryonic development in utero. If selection favors increasingly longer periods of egg retention, eventually the population will ~ontain females which give birth to live young. This model is not unique to our paper, but we have extended it as well as tested it. Both theory and data suggest that two factors, cold environments and maternal care of eggs, independently select for egg retention. Of these only cold climate seems to favor the full transition to live-bearing; brooding merely facilitates the transition. Cold climate has often been proposed as a major factor favoring the evolution of live-bearing (Mell 1929; Weekes 1935; Sergeev 1940: Packard 1966: Greer 1966; Packard et al. 1977). Sergeev even contended that cold climate was the single major force in the evolution of squamate live-bearing, although he did not rule out all other ecological factors (e.g., aquatic habitats), merely regarding them as having small overall effects. This study supports Sergeev's contention that cold is the major force, but his case can perhaps be made more strongly, because origins of live-bearing outside of cold environments seem to be rare. A demonstrative case is provided by brooding. which readily leads to egg retention. If many factors even weakly selected for live-bearing, then we would expect brooding to enhance this selection so that at least some origins of live-bearing would not occur ~ncold climates. Yet, at least six of the eight recent origins of live-bearing in brooding genera have been in cold climates, and perhaps all of them are (one genus unknown, one-half the examples of another genus inhabit cold climates). We have emphasized two somewhat different reasons why cold may be important EVOLUTION OF LIVE-BEARING 917 in the evolution of live-bearing: (a) Cold may injure the embryos at the time of laying; (b) cold may slow development so that hatching occurs later than is optimal. Hypothesis (a) requires that ground temperatures at the time of ovulation must be Iow enough to harm the embryos. This is directly testable on a species-by-species basis, but there is no universal temperature minimum which can be considered injuriously cold. Ground temperatures which are lethal to eggs of a tropical species may be warm by temperate standards. For example, eggs of a tropical iguana, which develop normally at 30° C, cannot tolerate even a week's exposure to 20° C (Licht and Moberly 1965). Twenty degrees C is not lethal to eggs of some temperate species (Sergeev 1940). Hypothesis (b) is very general because it argues an advantage for egg retention whenever the ground is cooler than the mother and the young benefit by earlier hatching. Early hatching could be advantageous for various reasons in seasonal environments, such as seasonal food availability or the approach of winter (Packard et al. 1977). Such generality might limit the usefulness of the cold climate hypothesis (b) were it not for a qualification. The cost of retaining eggs is likely to be proportional to the duration of retention, whereas the benefit depends upon how much the offspring's development is accelerated. A long duration of retention will have little effect on development time if the ground is only slightly cooler than the mother. Thus, environments which are cold by other standards (harmful to embryogenesis) are the ones likely to provide the most benefit from egg retention. There is one critical test of the above cold-climate hypotheses that may be feasible. Hypotheses (a) and (b) cannot explain egg retention in a female that lays several clutches per season, unless it is only the first and/or last clutch that is retained. If egg retention is found in such a female, then there is likely a nonthermoregulatory basis for its evolution. "' The strong correlation between cold climate and origin of live-bearing does not indicate that we have anticipated the correct reason for the correlation. Although we and others have suggested that cold climate is the evolutionary cause oflive-bearing, it could be that cold climate merely correlates with some other factor that is a more direct cause of live-bearing or that cold climate is indeed the cause but that we have misinterpreted how it selects for live-bearing. For example, Tinkle and Gibbons (1977) suggest that the evolution of live-bearing in cold environments may not have a thermoregulatory basis. Instead they suggest that cold climates (i) are variable, so that eggs in a nest face many unpredictable sources of mortality, and (ii) lengthen development. thus exposing the eggs to even more sources of mortality than otherwise. In the Tinkle and Gibbons model, retention evolves to shorten the interval in the nest, not necessarily to shorten the total incubation time. Further elucidation of these alternative hypotheses requires detailed studies on species with egg retention, but at present there is circumstantial evidence in favor of the thermoregulatory hypothesis (h) for three species, Lacerta muralis, L. viridis (Cooper 1965), and Natrix "at,.i" (Smith 1973). All three species show the intermediate stages of egg retention and all inhabit environments so cold that there is insufficient time to permit spring-laid eggs to hatch before winter. Natrix natrix not only shows lengthy egg retention. but also nests in compost heaps, the warmest available microhabitat. Despite this, eggs do not hatch before winter if the summer is cold (Smith 1973). 918 THE AMERICAN NATURALIST SUMMARY Most reptiles lay eggs, but many lizards and snakes give birth to live young by retaining the eggs within the oviducts until birth. The origin of live-bearing in reptiles is investigated here by posing a theoretical model and te.l>tingthe model with published data. Predictions are (1) that live-bearing should evolve in cold environments and (2) that maternal care of the eggs facilitates the evolution of live-bearing. Analyses of data from over 1,000species of lizards and snakes reveal that live-bearing has evolved recently at least 38 times, and an additional 60 species show the intermediate evolutionary stages (egg retention). Tests of these data support the predictions: Species which have recently evolved live-bearing or show the intermediate stages are much more likely to be found in cold climates or have maternal care of eggs than are squamates in general. The presentation in this paper differs from those of most earlier workers in distinguishing the cases in which live-bearing arises from the cases in which a live-bearing species radiates and invades new habitats. ACKNOWLEDGMENTS We dedicate this paper to Henry S. Fitch (University of Kansas). Without his pioneering work on reptilian life histories, and particularly his 1970 review of squamate reproduction. the present study would not have been feasible. Raissa L. Berg (University of Wisconsin) kindly translated the paper by Sergeev (1940) from Russian to English. We thank Donald W. Tinkle for encouragement, useful suggcstions on an earlier manuscript, and for a copy of an unpublished manuscript. We are also grateful to H. S. Fitch, O. Cuellar, E. L. Charnov. G. H. Pykc, J. M~'Legler, G. C. Packard, S. N. Salt he. A. E. Greer, and J. H. Werren for their comments. We gratefully acknowledge the support of a University of Utah Posdoctoral Fellowship (to RS) and a University of Utah Research Fellowship (to .18). We thank Toni Kinser for typing the manuscript. APPENDIX THE EVOLUTION OF EGG RETENTION It is useful to consider a model which incorporates changes in fecundity and survival to understand how selection acts on the evolution of egg retention. Since this paper deals with reptiles, the model incorporates assumptions which approximate the natural history of reptiles: overlapping generations with reproduction at regular intervals. Each reproduction is limited to one clutch of eggs, and we further assume that adult survival and fecundity are independent of age. The average fecundity of a female in such a population can be represented by the series Ra = sb + _ 2 sb spb + sp b + .. . = I -, -p (AI) in which s is juvenile survival from laying to first reproduction, b is fecundity in daughters, and p is adult survival from one reproduction to the next (e.g., Wilson and Bossert 1971). In a population constant in number, fecundity (Ro) is a measure of fitness, and it can be shown that a rarc dominant gene which increases Ro in females (having no effect on sex ratio or male fertility) will increase in frequency (technique in Charnov 1979). Thus, we have the intuitive result that selection in a stable population favors a gene which increases fecundity. In the EVOLUTION OF LIVE-BEARING notation of (AI), fecundity increases if s'b' ->l-p'l-p' sb , b' s li>s 919 or 1- p' I-p' (A2) with primes indicating the parameters of the rare type. Result (A2) is at least qualitatively applicable to the evolution of egg retention. 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