Printer Friendly

The evolution of oviparity with egg guarding and viviparity in lizards and snakes: a phylogenetic analysis.

Most species of lizards and snakes bury their eggs and do not guard them (Brattstrom 1974; Shine 1988). Egg guarding by females occurs in about 0.8% of species (Greer 1971; Shine 1988). Viviparity occurs in about 20% of all species (Blackburn 1982), and about 71% of the viviparous species belong to either the lizard families Iguanidae or Scincidae, or the snake families Colubridae or Viperidae. Thus, viviparity is distributed discontinuously among the squamate taxa, and families vary greatly in their proportions of viviparous species. This observation supports the hypothesis that selective pressures, preadaptations, and constraints vary at high taxonomic levels (Blackburn 1985). However, both oviparity with egg guarding and viviparity sometimes cooccur in the same lineages, suggesting a possible relationship between the evolution of viviparity and egg guarding (Shine and Bull 1979; Gross and Shine 1981; Shine 1985, 1988). Although several papers have considered the evolution of viviparity in squamates (Tinkle and Gibbons 1977; Shine and Bull 1979; Guillette et al. 1980; Pilorge and Barbault 1981; Guillette 1981; Blackburn 1982; Shine 1985), only one has discussed the evolution of egg guarding (Shine 1988).

From these studies, two specific hypotheses have been suggested. First, egg guarding can be regarded as an alternative to viviparity (Fitch 1970; Packard et al. 1977). A relatively frequent association of viviparous species and oviparous species with egg guarding in the same taxon may be due to similar environmental conditions or species characteristics leading to two different solutions. Second, egg guarding may be an intermediate step in the evolution of viviparity (Shine and Bull 1979). This hypothesis is supported by the high frequency of viviparous species in taxa containing egg-guarding species, especially in snakes, and by an apparent tendency for prolonged uterine retention of eggs in brooding squamates (Shine 1985). Thus, Fitch (1970) proposed an evolutionary transition from oviparity without egg guarding to viviparity (O[approaches]V) or from oviparity without egg guarding to oviparity with egg guarding (O[approaches]G), whereas Shine and Bull (1979) proposed an alternative scenario implying the evolution sequence from oviparity without egg guarding to oviparity with egg guarding and then to viviparity (O[approaches]G[approaches]V). If Fitch (1970) is correct, we expect to see a statistical difference between O[equivalence]V, O[equivalence]G transitions and G[equivalence]V transitions taking into account the number of respective cases of oviparity, viviparity, and egg guarding, whereas if Shine and Bull's (1979) hypothesis is right, we expect a statistical difference between G[approaches]V and V[approaches]G transitions. Our goal in this paper is to study in a phylogenetic context the evolution of viviparity and egg guarding in lizards and snakes to test Fitch's and Shine and Bull's hypotheses. Both hypotheses make the implicit assumptions that character evolution is irreversible and that oviparity with egg guarding and viviparity are derived. In our analysis, the irreversibility was tested, and the three reproductive modes were allowed to reverse freely.

MATERIALS AND METHODS

We followed the majority of workers on reproductive modes and classified species as either "oviparous" (shelled eggs are laid) or "viviparous" (the young are fully formed at laying; Budker 1958; Hoar 1969; Blackburn 1982, 1985). As egg-guarding behavior takes diverse forms in Squamata (lizards and snakes), following Shine (1988), we defined "egg guarding" as any form of postovipositional parental behavior or any action of the parent after oviposition that increases the chances of survival of the offspring. All species were therefore classified as (1) oviparous without egg guarding [TABULAR DATA FOR TABLE 1 OMITTED] (O), (2) oviparous with egg guarding (G), or (3) viviparous (V).

Phylogenetic and reproductive data were gathered from the literature (see references in Table 1). We analyzed only taxa showing all three reproductive modes. Consequently, the number of times they appeared in our sample is different than that recorded in the literature. When estimates of phylogenetic relationships were available, all taxonomic levels at which transitions were detected were employed for the analysis. For example, in Anguidae, we analyzed transitions occurring (1) among species within two genera (Diploglossus and Elgaria), (2) among genera or species within two subfamilies (Diploglossinae and Gerrhonotinae; Anguininae was excluded because all species are viviparous) and, (3) among all subfamilies, genera, or species within the family. We analyzed phylogenetic relationships (1) of the lizard and snake families; (2) within eight families (Boidae, Colubridae, Elapidae, Typhlopidae, Viperidae, Anguidae, Iguanidae, and Scincidae); (3) within ten subfamilies (Alsophiinae, Colubrinae, Natricinae, and Psammophiinae for Colubridae; Viperinae and Crotalinae for Viperidae; Diploglossinae and Gerrhonotinae for Anguidae; and Lygosominae and Scincinae for Scincidae); and (4) within seven genera (Elaphe and Natrix for Colubridae; Agkistrodon and Trimeresurus for Viperidae; Diploglossus and Elgeria for Anguidae; and Eumeces for Scincidae). Finally, when several cladograms were available for a taxon, we used all of them to analyze the sensitivity of our results with respect to possible misclassifications. As the irreversibility was tested, the character in the transformation series was considered as unordered (Fitch Parsimony). We used McClade (Maddison and Maddison 1990) for analyzing all phylogenies and studying character evolution. We used the cycling option to look for all possible reconstructions of the life-history character [ILLUSTRATION FOR FIGURE 1 OMITTED]. To infer polarity among reproductive characters, we used outgroup comparisons (Farris 1982; Maddison et al. 1984; Wiley et al. 1991). To use this method, it is necessary that the studied group (ingroup) be monophyletic because members of a monophyletic group are bound together by common ancestry relationships that they do not share with any other taxa (Brooks and McLennan 1991). The outgroup (any group used in an analysis not included in the taxon under study) is used for comparative purposes, usually in arguments concerning the relative polarity of characters (Wiley et al. 1991). To determine polarity, simple parsimony arguments are used in conjunction with an optimization routine developed by Maddison et al. (1984). These authors showed that hypotheses about the relationship among ingroup and outgroup(s) can have a profound influence on measures of character polarity.

RESULTS

Phylogenetic Analyses of the Familial Level

For lizards, we used phylogenetic data from Camp (1923), Underwood (1957, 1971), Northcutt (1978), Schwenk (1988), Estes and Pregill (1988), Estes et al. (1988), Presch (1988), Rieppel (1988), Greene (1988), and Greer (1989). For snakes, we used data from Rage (1987), McDowell (1987), Rieppel (1988), Greene (1988), and Cadle (1987, 1988).

Among all phylogenetic trees of lizard relationships at the family level, a maximum of 21 transitions were identified depending on the tree and the reconstructions used. Among phylogenetic trees of snake relationships at the family level, a maximum of 16 transitions were identified. We found a maximum of 15 transitions from oviparity without egg guarding (O) to viviparity (V), 10 transitions from oviparity without egg guarding (O) to oviparity with egg guarding (G), 8 transitions from viviparity to oviparity (V[approaches]O), and 5 transitions from viviparity to oviparity with egg guarding (V[approaches]G, Table 2A). Within all cladograms of lizard relationships, oviparity without egg guarding represents the plesiomorphic condition, and egg guarding and viviparity the apomorphic conditions. For snakes, depending on the reconstructions, oviparity or viviparity represent the plesiomorphic conditions and egg guarding always the apomorphic condition. At this taxonomic level, no transitions from egg guarding to viviparity were found. Moreover, the results clearly show that viviparity appears earlier than egg guarding (Table 3).

Phylogenetic Analyses of the Generic Level

The data of lizards and snakes used for generic relationships are shown in Table 1B. Among all phylogenetic trees of generic relationships at the familial or interfamilial levels, a maximum of 26 transitions were identified for lizards and a maximum of 29 transitions were identified for snakes depending on the tree used. We found 15 transitions from O[approaches]V, 16 transitions from O[approaches]G, 8 transitions from G[approaches]O, 8 transitions from V[approaches]O, 6 transitions from V[approaches]G, and 2 transitions from G[approaches]V.

The two G[approaches]V transitions were detected in Cadle's (1988), and Rieppel's (1988; [ILLUSTRATION FOR FIGURE 2 OMITTED]) cladograms. The first case (Cadle 1988) is found in a tree based on albumin immunological distances, which is under debate (Savitsky 1980; McCarthy [TABULAR DATA FOR TABLE 2 OMITTED] 1985). Indeed, this tree assumes monophyly between 18 genera of colubrids, elapids, and viperids when it turns out to be not the case (Bogert 1943; Underwood 1967; McDowell 1969; Voris 1977; Cadle and Gorman 1981; Schwaner et al. 1985). In the second case, one G[approaches]V transition was found in one reconstruction of Gerrhonotinae phylogeny constructed by Rieppel (1988; [ILLUSTRATION FOR FIGURE 2 OMITTED]), but in all other phylogenetic trees proposed by Smith (1942), Tihen (1949), Stebbins (1958), Waddick and Smith (1974), Gauthier (1982; [ILLUSTRATION FOR FIGURE 3 OMITTED]), or Good (1988, [ILLUSTRATION FOR FIGURE 1 OMITTED]) no V[approaches]G transition nor vice-versa are found.

To summarize, cases of G[approaches]V transitions are rare, and these transitions occur only in trees that are still under debate. As at the family level, oviparity and viviparity represent in all cases except one the plesiomorphic characters and egg guarding the derived character (in 70.5% of all reconstructions, oviparity is the ancestral character; in 29.49%, it is viviparity; and in only 0.01%, it is egg guarding).

Phylogenetic Analyses of the Species Level

The data of lizards and snakes used for species relationships are shown in Table 1B. Among all phylogenetic trees [TABULAR DATA FOR TABLE 3 OMITTED] of species relationships at the generic, familial, or interfamilial levels, a maximum of 19 transitions were identified for lizards and a maximum of 29 transitions were identified for snakes, depending on the tree used and the different possible reconstructions (Table 2C). We found 16 transitions from O[approaches]V, 12 transitions from O[approaches]G, 11 transitions from V[approaches]O, 3 transitions from G[approaches]O, and 2 transitions from G[approaches]V.

The two G[approaches]V transitions were detected in a long phylogenetic tree of 56 species of Eumeces (Scincidae) based on morphological characteristics constructed by Taylor (1935). Several authors (Greer 1970; Hikida 1978) questioned Taylor's (1935) hypothesis and concluded that Eumeces is not monophyletic. In the phylogenetic tree proposed by Murphy et al. (1983), the relationships among 11 populations of five species from the North American fasciatus group of Eumeces do not show V[equivalences]G transitions. In this study, the authors chose as the outgroups two species of Eumeces to determine the evolutionary polarity of the reproductive modes of the fasciatus group of the Eumeces.

Thus, the results show at all taxonomic levels very few of G[approaches]V transitions (only 2% G[approaches]V versus 11% V[approaches]G transitions, Table 2). As in the cases of families and genera, oviparity and viviparity represent in all cases the plesiomorphic character states and egg guarding the derived character state (in 60% of all reconstructions, oviparity is the ancestral character; and in 40%, it is viviparity).

DISCUSSION

In total, a maximum of 141 independent transitions (73 O[equivalence]V, 49 O[equivalence]G, and 19 V[equivalence]G) were detected. As we consider only phylogenetic trees with taxa showing all three reproductive modes, the percentage of oviparous, viviparous, or egg-guarding families, genera, and species used in our analyses are different than those generally cited in the literature (for our analyses, the percentage of families, genera, and species being oviparous: 135 cases or 46%, viviparous: 100 cases or 33%, and egg guarding: 63 cases or 21%). Based on these numbers, we can calculate the probability of occurrence of each type of transitions under the hypothesis of independence among transition types ([Mathematical Expression Omitted]; P [less than] 0.001). In particular, there is a strong deficit in the transition between egg guarding to viviparity compared with viviparity to oviparity with egg guarding ([Mathematical Expression Omitted]; P [less than] 0.001). The hypothesis that egg guarding preadapted lizards to viviparity (Shine and Bull 1979) seems to have little support (only four "G[approaches]V" transitions).

All reconstructions with MacClade of the life-history character show that oviparity is the ancestral character in 73.6%, viviparity in 26.397%, and egg guarding in 0.003%. Viviparity and egg guarding arose independently several times in the evolution of lizards and snakes, and within cladograms of family relationships, viviparity usually appeared before egg guarding. Egg guarding is widespread only within a restricted number of phylogenetic lineages of squamates (Fitch 1970; Shine 1988). By parsimony, this suggests that egg guarding has evolved only once in each group, early in its history, and has been retained during subsequent speciations (Ridley 1983). However, the transition from oviparity to viviparity does not seem to be as irreversible as we first thought. A hybridization experiment between oviparous and viviparous populations of Lacerta vivipara was conducted by Heulin et al. (1989). Numerous fertile [F.sub.2] hybrids were obtained, implying that there is no reproductive isolation between the two forms. Moreover, if egg guarding facilitates the evolution of viviparity, we might expect that species with mixed reproductive modes, such as L. vivipara, would have some oviparous populations with egg guarding and some viviparous ones. Among the 11 species within the families studied here showing more than one reproductive mode, all are either oviparous without egg guarding or viviparous.

Without underestimating the fact that viviparity is relatively easier to detect than is egg guarding, which depends on detailed field studies, all results suggest that egg guarding probably appeared more recently in the history of each taxon than did viviparity. Thus, our results are more consistent with Fitch's (1970) prediction that egg guarding probably did not evolve as an evolution history to viviparity than with Shine and Bull's hypothesis of guarding as an intermediate condition. That some transitions were observed between egg guarding and viviparity seems to be open to another interpretation. Although a complete analysis of the factors influencing the evolution of viviparity and egg guarding was not the goal of our study, we will consider a few hypotheses particularly relevant to lizards and snakes.

Environmental conditions that favor high maternal investment (viviparity, egg guarding, and even uterine retention of eggs) might influence the evolution of any of these strategies. Hence, the cooccurences in eight families (Boidae, Colubridae, Elapidae, Typhlopidae, Viperidae, Anguidae, Iguanidae, and Scincidae) of egg guarding and viviparous species may relate to common causation rather than to one factor (egg guarding) preadapting a species for another (viviparity).

Cold climates seem to have been the most important single selective agent favoring viviparity (Shine 1988), but it is equally obvious that this single force cannot explain all cases. For example, viviparity in Lygosoma or Sphenomorphus is not explainable by the cold-climate hypothesis (Shine 1988; Shine and Guillette 1988). Other hypotheses for the effects of environmental influences (e.g., hot climates, unpredictability of environment, and soil moisture) or species characteristics (e.g., nest predation and physiological constraints) either have not been tested (lack of data) or are unlikely to have general importance (Shine 1988).

In contrast to their effect on the evolution of viviparity, cold climates are not an important factor favoring egg guarding (Shine 1988). One factor that may promote the evolution of egg guarding is limited availability of nest sites (Shine 1988). If nest sites are scarce relative to the number of nesting females, older nests are likely to be excavated and destroyed by other females. Active defense of nest sites by females occurs in iguanines and is correlated with nest site availability (Wiewandt 1982). Although the limited availability of nest sites is consistent with egg guarding in Iguanidae, it is unlikely to be of general importance, because scarcity of suitable nesting sites may be a rare phenomenon (Shine 1988).
TABLE 4. Body-size means (snout-vent length) between oviparous and
viviparous species or between oviparous and egg-guarding species
within a genus. In parentheses is the number of species for which
size and reproductive data are available in the literature. O,
oviparity without egg guarding; G, oviparity with egg guarding; and
V, viviparity.


                                                Egg         Ratio
                    Oviparous   Viviparous   guarding
                      (cm)         (cm)         (cm)     V/O
G/O


Anguidae


Elgeria              354 (2)      232 (1)     369 (1)    0.65
1.04
Ophisaurus           505 (1)                  930 (4)
1.84


Chamaeleonidae


Chamaeleo            187 (7)       85 (4)                0.45


Iguanidae


Liolaemus             68 (1)       89 (9)                1.32
Phrynosoma           110 (8)      106 (2)                0.96
Sceloporus           168 (2)      202 (6)                1.20
Cyclura              225 (1)                  471 (2)    2.09


Scincidae


Eumeces               62 (5)       62 (6)      75 (2)    1.00
1.20
Scelotes             180 (2)      138 (1)                0.77
Harrisoniascincus     56 (1)       45 (1)                0.80
Typhlosaurus         285 (2)      153 (2)                0.54
Leiolopisma           66 (6)       57 (1)                0.86
Anamolopus           127 (3)      102 (1)                0.80
Glaphyromorphus       61 (7)       72 (1)                1.17
Lerista               62 (2)       59 (3)                0.95
Mabuya               132 (1)      135 (1)                1.02


Varanidae


Varanus              313 (2)                  544 (3)
1.74


Boidae


Python               180 (1)                  595 (4)
3.30


Colubridae


Elaphe               158 (3)                  220 (3)
1.39
Heterodon             75 (2)                  116 (1)
1.55
Lampropeltis         133 (5)                  199 (1)
1.50


Elapidae


Naja                 210 (3)                  270 (2)
1.28


Viperidae


Causus                44 (1)                  100 (1)
2.27
Vipera               145 (2)       73 (7)                0.50


Although the same ecological factors may explain the appearance of both egg guarding and viviparity, the evolution of correlated traits that favor or are linked to their appearance could be quite different. In particular, a major benefit of egg guarding is the repulsion of potential egg predators, then egg guarding should evolve most often in species in which the parent is capable of deterring predators (Shine 1988). This is most likely in large species. To test the hypothesis that large size cooccurs with egg guarding, we have taken the mean snout-vent length for each mode, and using within-genera, pairwise comparisons, we can calculate size differences between O and V, and O and G (Felsenstein 1985; Burt 1989; Harvey and Pagel 1991; Table 2). Our results show that egg guarding is associated with an increase in size ([t.sub.11] = -5.96; P [less than] 0.001, one-tailed test). Although viviparity is associated with a reduction in size ([t.sub.15] = 2.00; P [less than] 0.035, one-tailed test). The small size of viviparous species may be explained by the benefits of viviparity in terms of an increase in the number of surviving offspring (Neil 1964). In this case, size might relate to the decrease of a viviparous female's fecundity. On the contrary, reduction in fecundity in viviparous species could have been linked in a reduction in size (Dunham et al. 1988). The increase in size of egg guarding species is consistent with the prediction that this behavior should be found most often in groups in which parents are able to defend their eggs. Although this latter result may explain why egg guarding and viviparity seem to be independent, almost antagonistic, evolutionary events, a similar analysis on a larger sample size and using more life-history traits would be necessary to fully support this prediction.

LITERATURE CITED

Alvarez del Toro, M. 1960. Reptiles de Chiapas. Publicaciones del Instituto Zoologico del Estado, Tuxtla Gutierrez, Chiapas.

Amaral, A. 1977. Contribuicao a biologia dos brasileiros (reproduccao). Col. Trab. Institut. Butantan 2:185-187.

Andren, C., and G. Nilson. 1979. Vipera latifii (Reptilia, Serpentes, Viperidae) an endangered viper from Lar Valley, Iran, and remarks on the sympatric herpetofauna. Journal of Herpetology 13:335-341.

Arnold, E. N., and A. E. Leviton. 1977. A revision of the lizard genus Scincus (Reptilia: Scincidae). Bulletin of the British Museum Natural History Zoology 31:189-248.

Barbour, T., and C. T. Ramsden. 1919. The herpetology of Cuba. Memoirs of the Museum of Comparative Zoology (47) 2:69-213.

Baverstock, P. R., and S. L. Donnellan. 1990. Molecular evolution in Australian dragons and skinks: a progress report. Memoirs of the Queensland Museum 29:323-331.

Blackburn, D. G. 1982. Evolutionary origins of viviparity in the reptilia. I. Sauria. Amphibia-Reptilia 3:185-205.

-----. 1985. Evolutionary origins of viviparity in the Reptilia. II. Serpentes, Amphisbaenia, and Ichthyosauria. Amphibia-Reptilia 6:259-291.

Bogert, C. M. 1943. Dentitional phenomena in cobras and other elapids with notes on adaptive modifications of fangs. Bulletin of the American Museum of Natural History 81:285-360.

Brain, C. K. 1959. Note on the breeding of the South African skink, Typhlosaurus lineatus Boulenger. Copeia 1959:70-71.

Brattstrom, B. H. 1964. Evolution of the pit vipers. Transactions of the San Diego Society of Natural History 13(11): 185-268.

-----. 1974. The evolution of reptilian social behavior. American zoology 14:35-49.

Broadley, D. G. 1968. Revision of the African genus Typhlosaurus Wiegmann (Sauria:Scincidae). Arnoldia (Rhodesia) (3)36:1-20.

Brooks, D. R., and D. A. McLennan. 1991. Phylogeny, ecology, and behavior. A research program in comparative biology. University of Chicago Press, Chicago.

Budker, P. 1958. La viviparite chez les Selaciens. Pp. 1755-1790 in P. P. Grasse, ed. Traite de Zoologie 13, 2. Masson, Paris.

Burt, A. 1989. Comparative methods using phylogenetically independent constraints. Oxford Surveys in Evolutionary Biology 6:33-53.

Cadle, J. E. 1987. The geographic distribution of snakes. Pp. 77-105 in R. A. Seigel, J. T. Collins, and S. S. Novak, eds. Snakes: ecology and evolutionary biology. Macmillan, New York.

-----. 1988. Phylogenetic relationships among advanced snakes: a molecular perspective. University of California Press, Berkeley, CA 119:1-77.

Cadle, J. E., and G. C. Gorman. 1981. Albumin immunological evidence and the relationships of sea snakes. Journal of Herpetology. 15:329-334.

Camp, C. 1923. Classification of the lizards. Bulletin of the American Museum of Natural History 48:289-481.

Carey, W. M. 1975. The rock iguana, Cyclura pinguis, on Anegada, British Virgin Islands, with notes on Cyclura ricordi and Cyclura cornuta on Hispaniola. Bulletin of the Florida State Museum, Biological Science 19:189-233.

Carpenter, C. C. 1966. The marine iguana of the Galapagos Islands, its behavior and ecology. Proceedings of the California Academy of Sciences 34:329-376.

Cole, C. J. 1978. Karyotype and systematics of the lizards in the variabilis, jelapae, and scalaris species groups of the genus Sceloporus. American Museum Novitates 2653:1-13.

Conant, R., and A. Downs. 1940. Miscellaneous notes on the eggs and young of reptiles. Zoologica 25:33-48.

Cooper, W. E., L. J. Vitt, L. D. Vangilder, and J. W. Gibbons. 1983. Natural nest sites and brooding behavior of Eumeces fasciatus. Herpetologica 14:65-66.

Daniel, J. C. 1983. The book of Indian reptiles. Bombay Natural History Society 13:1-57.

Deoras, P. J. 1978. Snakes of India, 3rd review. National Book Trust, New Delhi.

Donoso-Barros, R. 1966. Reptiles de Chile. Edicion de la Universidad, Santiago, Chile.

Duellman, W. E. 1978. The biology of an equatorial herpetofauna in Amazonian Ecuador. University of Kansas Museum of Natural History, Miscellaneous Publication 65:1-352.

-----. 1979. The numbers of amphibians and reptiles. Herpetological Review 10:83-84.

Dunham, A. E., D. B. Miles, and D. N. Reznick. 1988. Life history patterns in squamate reptiles. Pp. 441-522 in C. Gans and R. B. Huey, eds. Defense and life history. Biology of the reptilia, vol. 16. Alan R. Liss, New York.

Estes, R., and G. Pregill. 1988. Phylogenetic relationships of the lizard families. Stanford University Press, Stanford, CA.

Estes, R., K. De Queiroz, and J. Gauthier. 1988. Phylogenetic relationships within squamata. Pp. 119-270 in R. Estes and G. Pregill, eds. Phylogenetic relationships of the lizard families. Stanford University Press, Stanford, CA.

Etheridge, R., and K. De Queiroz. 1988. A phylogeny of Iguanidae. Pp. 283-337 in R. Estes and G. Pregill, eds. A phylogeny of the lizard families. Stanford University Press, Stanford, CA.

Farris, J. S. 1982. Outgroups and parsimony. Systematic Zoology 31:328-334.

Felsenstein, J. 1985. Phylogenics and the comparative method. American Naturalist 125:1-15.

Fitch, H. S. 1954. Life history and ecology of the five-lined skink, Eumeces fasciatus. University of Kansas Publications of the Museum of Natural History 8:1-156.

-----. 1970. Reproductive cycles in lizards and snakes. University of Kansas Publications of the Museum of Natural History 52:1-247.

Frost, D. R., and R. Etheridge. 1989. A phylogenetic analysis and taxonomy of Iguanian lizards (Reptilia: Squamata). University of Kansas Publications of the Museum of Natural History 81:1-47.

Fukada, H. 1978. Growth and maturity of the Japanese rat snake, Elaphe climacophora (Reptilia, Serpentes, Colubridae). Journal of Herpetology 12:269-274.

Garland, T. J., R. B. Huey, and A. F. Bennett. 1991. Phylogeny and coadaptation of thermal physiology in lizards: a reanalysis. Evolution 45:125-131.

Gauthier, J. 1982. Fossil Xenosauridae and Anguidae from the Lower Eocene Wasatch Formation, southcentral Wyoming, and a revision of the Anguioidea. Contribution to Geology, University of Wyoming, 21(1):7-54.

Goldberg, S. R. 1971. Reproduction in the short horned lizard Phrynosoma douglassi in Arizona. Herpetologica 27:311-314.

Good, D. A. 1988. Phylogenetic relationships among Gerrhonotine lizards. An analysis of external morphology. University of California Publications in Zoology 121:1-103.

Greene, H. W. 1988. Antipredator mechanisms in reptiles. Pp. 1-153 in C. Gans and R. B. Huey, eds. Biology of the reptilia, defense and life history. vol. 16. Alan R. Liss, New York.

Greer, A. E. 1967. Notes on the mode of reproduction in Anguid lizards. Herpetologica (23)2:91-98.

-----. 1970. A subfamilial classification of Scincid lizards. Bulletin of the Museum of Comparative Zoology 139:151-183.

-----. 1971. Crocodilian nesting habits and evolution. Fauna 2: 20-28.

-----. 1974. The generic relationships of the Scincid lizard genus Leiolopisma and its relatives. Australian Journal of Zoology Supplementary Series 31:1-67.

-----. 1977. The systematics and evolutionary relationships of the Scincid lizard genus Lygosoma. Journal of Natural History 11:515-540.

-----. 1979. A phylogenetic subdivision of Australian skinks. Records of the Australian Museum 32:339-371.

-----. 1989. The biology and evolution of Australian lizards. Surrey Beatty, Australia.

Gross, M. R., and R. Shine. 1981. Parental care and mode of fertilization in ectothermic vertebrates. Evolution 35:775-793.

Guillette, L. J. 1981. On the occurrence of oviparous and viviparous forms of the Mexican lizard Sceloporus aeneus. Herpetologica 37:11-15.

Guillette, L. J., R. E. Jones, K. T. FitzGerald, and H. M. Smith. 1980. Evolution of viviparity in the lizard genus Sceloporus. Herpetologica 36:201-215.

Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford Series in Ecology and Evolution, Oxford University Press, Oxford.

Heulin, B., M. J. Arrayago, and A. Bea. 1989. Experience d'hybridation entre les souches ovipare et vivipare du lezard Lacerta vivipara. Comptes rendus de l'Academie des Sciences, Paris. 308:341-346.

Hikida, T. 1978. Problems of distribution and systematics of the genus Eumeces in East Asia. Acta Phytotaxonomica Geobotanica 29:144-148.

-----. 1981. Reproduction of the Japanese skink (Eumeces latiscutatus). Zoological Magazine (Tokyo) 90:85-92.

Hoar, W. S. 1969. Reproduction. Pp. 94-121 in W. S. Hoar and D. J. Randall. Fish physiology. Academic Press, New York.

Hutchinson, M. N., S. L. Donnellan, P. R. Bayerstock, M. Krieg, S. Simms, and S. Burgin. 1990. Immunological relationships and generic revision of the Australian lizards assigned to the genus Leiolopisma (Scincidae; Lygosominae). Australian Journal of Zoology 38:535-554.

Iverson, J. B. 1979. Behavior and ecology of the rock iguana Cyclura carinata. Bulletin of the Florida State Museum, Biological Sciences 24:175-358.

Jansen, F. J., and G. L. Paukstis. 1991. A preliminary test of the adaptative significance of environmental sex determination in reptiles. Evolution 45:435-440.

Kluge, A. 1991. Boine snakes phylogeny and research cycles. Miscellaneous Publications Museum of Zoology University of Michigan 178:1-55.

Koba, K., K. Tandku, E. Nakamoto, and H. Morimoto. 1970. The eggs of the Tokaru habu (Trimeresurus tokarensis): Condition in the oviduct, laying, and hatching. Snake 2:32-38.

Kuntz, R. E. 1963. Snakes of Taiwan. Quarterly Journal of the Taiwan Museum 16:1-81.

Langerwerf, B. 1981. The southern alligator lizard Gerrhonotus multicarinatus Blainville 1935: its care and breeding in captivity. British Herpetological Society Bulletin 4:21-25.

Lowe, C. H., and C. W. Howard. 1975. Viviparity and reproductive pattern in Phrynosoma ditmarsi in Sonora, Mexico. Southwestern Naturalist 20:265-270.

Maddison, W. P., and D. R. Maddison. 1990. MacClade Sinauer, Sunderland, MA.

Maddison, W. P., M. J. Donoghue, and D. R. Madalison. 1984. Outgroup analysis and parsimony. Systematic Zoology 33:83-103.

Marx, H., and G. R. Rabb. 1965. Relationships and zoogeography of the viperine snakes (family: Viperidae). Fieldana, Zoology 44:161-206.

McCarthy, C. J. 1985. Monophyly of Elapid snakes (Serpentes: Elapidae): an assessment of the evidence. Zoological Journal of the Linnean Society 83:79-93.

McConkey, E. H. 1954. A systematic study of the North American lizards of the genus Ophisaurus. American Midland Naturalist 51:113-171.

McCoy, C. J. 1968. Reproductive cycles and viviparity in Guatemalan Corytophanes pericarinatus (Reptilia, Iguanidae). Herpetologica 24:175-178.

McDowell, S. B. 1969. Notes on the Australian sea snakes Ephalophis greyi (Serpentes, Elapidae: Hydrophiinae) and the origin and classification of sea snakes. Zoological Journal of the Linnean Society 48:333-349.

-----. 1979. A catalogue of the snakes of New Guinea and the Solomons, with special reference to those in the Bernice P. Bishop Museum. Boinae and Acrochordoidea (Reptilia, Serpentes). Journal of Herpetology 13:1-92.

-----. 1987. Systematics. Pp. 3-50 in R. A. Seigel, J. T. Collins, and S. S. Novak, eds. Snakes: ecology and evolutionary biology. Macmillan, New York.

Mengden, G. A. 1985a. A chromosomal and electrophoretic analysis of the genus Pseudonaja. Pp. 193-208 in G. Grigg, R. Shine, and H. Ehmann, eds. Biology of Australian frogs and reptiles. Surrey Beatty and The Royal Zoological Society of New South Wales, Australia.

-----. 1985b. Australian Elapid phylogeny: a summary of the chromosomal and electrophoretic data. Pp. 185-192 in G. Grigg, R. Shine, and H. Ehmann, eds. Biology of Australian frogs and reptiles. Surrey Beatty and The Royal Zoological Society of New South Wales, Australia.

Mishima, S., Y. Sawai, S. Yamamoto, and K. Sawai. 1977. Studies on a natural monument, Shirohebi albino (Elaphe climacophora) on the Iwakuni in Japan. Observations on copulation, egg-laying, and hatching of the Shirohebi. Snake 9:14-26.

Montanucci, R. R. 1979. Notes on systematics of horned lizards allied to Phrynosoma orbiculare (Lacertilia: Iguanidae). Herpetologica 35:116-124.

Murphy, J. B., D. G. Barker, and B. W. Tryon. 1978. Miscellaneous notes on the reproductive biology of reptiles. Eleven species of the family Boidae, genera Candoia, Corallus, Epicrates, and Python. Journal of Herpetology 12:385-390.

Murphy, R. W., W. R. Cooper, and W. S. Richardson. 1983. Phylogenetic relationships of the North American five-lined skinks, genus Eumeces (Sauria, Scincidae). Herpetologica 39:200-211.

Neil, W. T. 1964. Viviparity in snakes: some ecological and zoogeographical considerations. American Naturalist 48: 35-55.

Nickerson, M. A. 1974. Comments on the reproduction of Pope's pit viper (Trimeresurus popeorum Smith). Journal of Herpetology 5:451-452.

Noble, G. K., and E. R. Masson. 1933. Experiments on the brooding habits of the lizards Eumeces and Ophisaurus. American Museum Novitates 619.

Northcutt, G. 1978. Forebrain and midbrain organization in lizards and its phylogenetic significance. Pp. 77-491 in N. Greenberg and P. Maclean, eds. Behavior and neurology of lizards. National Institute of Health: Department of Health, Education, and Welfare, Publication ADM.

Packard, G. C., G. R. Tracy, and J. J. Roth. 1977. The physiological ecology of reptilian eggs and embryos and the evolution of viviparity within the class reptilia. Biology Review 52:71-105.

Piennar, U. (de V.), and V. F. M. FitzSimons. 1966. The reptile fauna of the Kruger National park. Koedoe, Monograph 1:1-223.

Pilorge, T., and R. Barbault. 1981. La viviparite chez les lezards: evolution et adaptation. Acta Oecologica 2:387-397.

Presch, W. 1969. Evolutionary osteology and relationships of the horned lizard genus Phrynosoma (family Iguanidae). Copeia 2: 250-275.

-----. 1988. Cladistic relationships within the Scincomorpha. Pp. 471-490 in R. Estes and G. Pregill, eds. Phylogenetic relationships of the lizard families. Stanford University Press, Stanford, CA.

Rage, J. C. 1987. Fossil history. Pp. 51-76 in R. A. Seigel, ed. Snakes, ecology, and evolutionary biology. Macmillan, New York.

Reitinger, F. F. 1978. Common snakes of South East Asia and Hong Kong. Heinemann, Hong Kong.

Ridley, M. 1983. The explanation of organic diversity: the comparative method and adaptations for mating. Oxford University Press, Oxford.

Rieppel, O. 1979. A cladistic classification of primitive snakes based on skull structure. Zoologische Systematik und Evolutionsforschung 17:140-150.

-----. 1988. The classification of the Squamata. Pp. 37-103 in M. J. Benton, ed. The phylogeny and classification of the Tetrapods, vol. 1. Amphibians, reptiles, birds. Systematics Association Special volume no 35a, Clarendon Press, Oxford.

Saint Girons, H., and G. Nauleau. 1981. Poids des nouveau-nes et strategies reproductrices des viperes europeennes. Revue d'Ecologie (Terre et Vie) 35:597-616.

Savitzky, A. H. 1980. The role of venom delivery strategies in snake evolution. Evolution 34:1194-1204.

Schmidt, K. P., and R. F. Inger. 1957. Living reptiles of the world. Hanover House, Garden City, NY.

Schwaner, T. D., P. R. Baverstock, H. C. Dessauer, and G. A. Mengden. 1985. Immunological evidence for the phylogenetic relationships of Australian Elapid snakes. Pp. 177-183 in G. Grigg, R. Shine, and H. Ehmann, eds. Biology of Australian frogs and reptiles. Surrey Beatty and The Royal Zoological Society of New South Wales, Australia.

Schwenk, K. 1988. Comparative morphology of the Lepidosaur tongue and its relevance to squamate phylogeny. Pp. 569-597 in R. Estes and G. Pregill, eds. Phylogenetic relationships of the lizard families. Stanford University Press, Stanford, CA.

Shaw, C. E. 1954. Captive-bred Cuban iguanas, Cyclura macleayi macleayi. Herpetologica 19:73-78.

Shine, R. 1985. The evolution of viviparity in reptiles: an ecological analysis. Pp. 605-694 in C. Gans and F. Billet, eds. Biology of the reptilia. Wiley, New York.

-----. 1988. Parental care in reptiles. Pp. 276-329 in C. Gans and R. B. Huey, eds. Biology of the reptilia. Alan R. Liss, New York.

Shine, R., and J. J. Bull. 1979. The evolution of live bearing in lizards and snakes. American Naturalist 113:905-923.

Shine, R., and L. J. Guillette. 1988. The evolution of viviparity in reptiles: a physiological model and its ecological consequences. Journal of Theoretical Biology 132:43-50.

Smith, H. M. 1939. The Mexican and central American lizards of the genus Sceloporus. Field Museum of Natural History, Zoology 25:1-397.

-----. 1942. Mexican herpetological miscellany: a tentative arrangement and key to Mexican Gerrhonotus, with the description of a new race. Proceedings of the United States Natural Museum 92:363-369.

Smith, H. M., and W. P. Hall. 1974. Contributions to the concepts of reproductive cycles and systematics of the scalaris group of the lizard genus Sceloporus. Great Basin Natural 34:97-104.

Smith, H. M., R. B. Smith, and H. L. Savin. 1977. A summary of snakes classification (Reptilia, Serpentes). Journal of Herpetology 11:115-121.

Smith, M. A. 1943. The fauna of British India. Reptilia and Amphibia, vol. 3. Serpentes. Taylor and Francis, London.

Stebbins, R. C. 1954. Amphibians and reptiles of western North America. McGraw-Hill, New York.

-----. 1958. A new alligator lizard from the Panamint Mountains, Inyo County, California' American Museum Novitates 1883:1-27.

Taylor, E. H. 1935. A taxonomic study of the cosmopolitan Scincoid lizards of the genus Eumeces with an account of the distribution and relationships of its species. University of Kansas Sciences Bulletin 23:1-643.

-----. 1956. A review of the lizards of Costa Rica. University of Kansas Sciences Bulletin 38:1-322.

Thomas, R. A., and J. Dixon. 1976. A re-evaluation of the Sceloporus scalaris group (Sauria: Iguanidae). Southwestern Naturalist 20:523-536.

Tihen, J. A. 1949. The genera of Gerrhonotine lizards. American Midland Naturalist 41:580-601.

Tinkle, D. W., and J. W. Gibbons. 1977. The distribution and evolution of viviparity in reptiles. Miscellaneous Publication of the Museum of Zoology of the University of Michigan 154:1-55.

Trillmich, K. 1979. Feeding behaviour and social behaviour of the marine iguanas. Noticias de Galapagos 29:19-20.

Underwood, G. 1957. On lizards of the family Pygopodidae: contribution to the morphology and phylogeny of the squamata. Journal of Morphology 100:207-268.

-----. 1967. A contribution to the classification of snakes. Trustees of the British Museum (Natural History) London 653:1-179.

-----. 1971. A modern appreciation of Camp's classification of the lizards. Introduction to reprint of C. Camp's classification of the lizards. Herpetological Society Study, Amphibian and Reptiles VII-XVII.

-----. 1976. Morphology and biology of reptiles. Pp. 151-175 in A. Bellairs and C. B. Cox eds. Linnean Society Symposium Series 3:151-175.

Underwood, G., and A. Stimson. 1990. A classification of Pythons (Serpntes, Pythoninae). Journal of Zoology London 221:565-603.

Vitt, L. J. 1987. Communities. Pp. 335-365 in R. A. Seigel, J. T. Collins, and S. S. Novack, eds. Snakes, ecology, and evolutionary biology. Macmillan, New York.

Voris, H. K. 1977. A phylogeny of the sea snakes (Hydrophiidae). Fieldiana, Zoology 70:79-169.

Waddick, J. W., and H. M. Smith. 1974. The significance of scale characters in evaluation of the lizard genera Gerrhonotus, Elgeria, and Barisia. Great Basin Naturalist 34:257-266.

Wallach, V. 1985. A cladistic analysis of the terrestrial Australian Elapidae. Pp. 223-243 in G. Grigg, R. Shine, and H. Ehmann, eds. Biology of Australian frogs and reptiles. Surrey Beatty limited in association with The Royal Zoological Society of New South Wales, Australia.

Wang, B. 1966. Studies on the ecology of four species of lizards in Hangchow. II. Breeding. Acta Zoologica Sinica 19:170-186.

Werner, Y. L. 1982. Observations on eggs of Eublepharid lizards with comments on the evolution of the Gekkoidea. Zoologische Mededelingen, Leiden 47:211-224.

Wiewandt, T. A. 1982. Evolution of nesting patterns in Iguanine lizards. Pp. 119-141 in G. M. Burghardt and A. S. Rand, eds. Iguanas of the world. Noyes Publication, Park Ridge, NJ.

Wiley, E. O., D. Siegel-Causey, D. R. Brooks, and V. A. Funk. 1991. The compleat cladist: a primer of phylogenetic procedures. University of Kansas Museum of Natural History 19:1-158.
COPYRIGHT 1996 Society for the Study of Evolution
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 1996 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:de Fraipont, M.; Clobert, J.; Barbault, R.
Publication:Evolution
Date:Feb 1, 1996
Words:6211
Previous Article:Postglacial range fluctuation, genetic subdivision and speciation in the western North American spotted frog complex, Rana pretiosa.
Next Article:Molecular genetic evidence for parallel life-history evolution within a Pacific salmon (sockeye salmon and kokanee, Oncorhynchus Nerka).
Topics:

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters