Evolution Of Viviparity In Reptiles Research Articles

Climatic niche evolution in the viviparous Sceloporus torquatus group (Squamata: Phrynosomatidae).

The cold-climate hypothesis maintains that viviparity arose as a means to prevent increased egg mortality in nests owing to low temperatures, and this hypothesis represents the primary and most strongly supported explanation for the evolution of viviparity in reptiles. In this regard, certain authors have stated that viviparous species will exhibit speciation via climatic niche conservatism, with similar climatic niches being observed in allopatric sister species. However, this prediction remains to be tested with bioclimatic variables relevant to each viviparous group. In the present study, we examined climatic niche evolution in a group of North American viviparous lizards to determine whether their diversification is linked to phylogenetic niche conservatism (PNC). We evaluated the phylogenetic signal and trait evolution of individual bioclimatic variables and principal component (PC) scores of a PC analysis, along with reconstructions of ancestral climate tolerances. The results suggest that diversification of the Sceloporus torquatus group species is associated with both niche differentiation and PNC. Furthermore, we did not observe PNC across nearly all bioclimatic variables and in PC2 and PC3. However, in Precipitation Seasonality (Bio15), in Precipitation of Coldest Quarter (Bio19) and in PC1 (weakly associated with variability of temperature), we did observe PNC. Additionally, variation of the scores along the phylogeny and Pagel’s delta (δ) >1 of PC3 suggests a fast, recent evolution to dry conditions in the clade that sustains S. serrifer.

Viviparity Advantages in the Lizard Liolaemus sarmientoi from the End of the World

Two hypotheses have prevailed to explain the evolution of viviparity in reptiles: the first proposed that viviparity evolved in response to cold-climates because the possibility of pregnant females to thermoregulate at higher temperatures than embryos could experience in a nest in nature. The second hypothesis posits that the advantage of viviparity is based on the possibility of females to maintain stable body temperatures during development, enhancing offspring fitness. With the aim to contribute to understanding the origins of viviparity in reptiles, we experimentally subjected pregnant females of the austral lizard Liolaemus sarmientoi to two temperature treatments until parturition: one that simulated environmental temperatures for a potential nest (17–25 °C) and another that allowed females to thermoregulate at their preferred body temperature (17–45 °C). Then, we analysed newborn body conditions and their locomotor performance to estimate their fitness. In addition, we measured the body temperature in the field and the preferred temperature in the laboratory of pregnant and non-pregnant females. Pregnant females thermoregulated to achieve higher temperatures than the environmental temperatures, and also thermoregulated within a narrower range than non-pregnant females. This could have allowed embryos to develop in higher and more stable temperatures than they would experience in a nest in nature. Thus, offspring developed at the female preferred temperature showed greater fitness and were born earlier in the season than those developed at lower environmental temperatures. Herein, we show that results are in agreement with the two hypotheses of the origin of viviparity for one of the southernmost lizards of the world.

Loss of Nesting Behavior and the Evolution of Viviparity in Reptiles

Loss of Nesting Behavior and the Evolution of Viviparity in Reptiles

Superficial lizards in cold climates: Nest site choice along an elevational gradient

AbstractEmbryonic conditions may limit the distributions of egg‐laying ectotherms, and recent research suggests that nesting mothers of wide‐ranging species may use a number of factors to compensate for differing climates. However, while variation in temporal factors across environmental gradients are common or pervasive (i.e. seasonal timing of nesting), similar evidence for spatial factors is rare (e.g. aspect, openness and depth of nest sites). I tested the idea that a wide‐ranging lizard, the Australia water dragon (Physignathus lesueurii), uses nest depth to counter climate differences along a temperature cline at their cold‐end range margin. Two measures of nest depth were significantly, inversely related to elevation across six populations spanning 700 m. Elevation explained 83–86% of the variation in nest depth. These findings support a thermal compensatory mechanism for this pattern, although soil moisture compensation is plausible. My results directly support a recent, untested prediction that the evolution of viviparity in reptiles is preceded by a behavioural shift towards increasingly superficial nest sites in cold climates, followed by selection for increased egg retention to avoid temperature extremes. However, in the present study egg desiccation rates increased with increasing elevation in a dry year, suggesting that increased egg retention may evolve in response to lethal hydric conditions, rather than lethal temperatures. When considered alongside recent research, the present study indicates that water dragons possess several mechanisms for adjusting to climate change.

EVOLUTION OF VIVIPARITY IN REPTILES: INTRODUCTION TO THE SYMPOSIUM

The Fifth World Congress of Herpetology, held in 2005 at the University of Stellenbosch (Republic of South Africa), provided an excellent opportunity to host a symposium on the evolution of viviparity in reptiles. Several symposia on viviparity have been held during the past 15 years, and these have yielded comprehensive reviews of squamates (e.g., Blackburn, 1993, 1998, 2000; Stewart, 1993; Stewart and Thompson, 2000, 2003; Thompson et al., 2000, 2004) and many other papers. However, most of these symposia were limited in scope to particular features (placental membranes, the oviduct) or aspects (morphology, physiology). The World Congress venue represented the first broad-based symposium to focus on viviparity in squamates, a taxon of special importance to biologists interested in viviparity. This symposium was multi-disciplinary, and integrated morphology, physiology, biochemistry, molecular biology, and evolutionary theory. The evolution of viviparity holds intrinsic interest for a number of reasons. First, humans are viviparous and have natural curiosity about their own reproduction. Second, mode of reproduction relates closely to a species’ ecology, physiology, and behavior, and is central to its life history strategy. Third, viviparity is a central, recurring theme in vertebrate history, and its existence raises fascinating functional and evolutionary questions. Squamate reptiles provide an excellent model system for studies on the evolution of viviparity because live-bearing reproduction has evolved in the Squamata at least 100 times (Blackburn, 1999), and complex placentae have evolved four or five times (Thompson and Speake, 2006). Many of the reptilian origins of viviparity have occurred at low taxonomic levels and in geologically recent times, potentially allowing a reconstruction of the transition to viviparity. Additionally, reptiles are amniotes, and their fetal membranes are homologous to those that contribute to mammalian placentae. Consequently, squamate reptiles arguably are the best available model for attempts to understand the evolution of mammalian reproduction. Nevertheless, squamates have a reptilian physiology as well as unique features (such as a yolk cleft and an isolated yolk mass), and the sequence by which viviparity and placentation evolved differs in squamates and mammals (Blackburn, 2006). Therefore, caution is required in applying conclusions from reptilian studies to mammalian systems. One mark of the growing maturity of the field is that studies on squamate viviparity are justified in their own right, aside from whatever insight they may give into mammals. This symposium addressed two related questions: how viviparity has evolved from oviparity, and how complex placentae have evolved from simple placentae. The symposium consisted of fifteen invited presentations, beginning with a review of the utility of reptiles to a more general model of the evolution of viviparity, followed by three papers on morphological details of extraembryonic and placental development and structure. Four papers described aspects of the physiology of maternal-embryonic interactions, including the occurrence of HoxA10 genes. The afternoon session began with a focus on eggs and oviparous species and the factors that may have led to or limited the evolution of viviparity, and concluded with a series of papers that covered diverse topics in ecology, morphology, and physiology. The symposium highlighted the rapid progress that has been made in understanding CORRESPONDENCE: e-mail, Mike.Thompson@bio.usyd. edu.au Herpetological Monographs, 20, 2006, 129–130 E 2006 by The Herpetologists’ League, Inc.

An empirical test of the `predictability' hypothesis for the evolution of viviparity in reptiles

Abstract Viviparity (live-bearing) has evolved from oviparity (egg-laying) >100 times in reptile phylogeny, but the selective forces responsible remain unclear. Tinkle & Gibbons (1977) proposed that prolonged uterine retention of eggs (leading ultimately to viviparity) is favoured by natural selection when it allows the reproducing female to better predict the incubation conditions that will occur in alternative potential nest-sites, and hence select the optimal site in which to deposit her eggs. This ingenious hypothesis has never been tested empirically. Over a 7-year period, I monitored temperatures inside 124 natural nests of egg-laying scincid lizards at three different elevations in the Brindabella Range of south-eastern Australia. As a measure of thermal predictability, I used correlation coefficients from comparisons of temperatures early vs. later in incubation among nests within each site. Both the mean and standard deviation of nest temperatures were examined in this way for each week through incubation. I performed these calculations under two models: one where the female assesses nest temperatures at the time of oviposition only, and one where she monitors temperatures constantly from the usual oviposition date until the actual time of laying. These analyses falsified two major assumptions of the ‘predictability’ hypothesis. First, nest temperatures at higher elevations were no less predictable than were those at lower elevations; instead, predictability was high in all situations. Secondly, a longer delay before oviposition decreased rather than increased the predictability of thermal conditions during subsequent incubation. I conclude that critical assumptions of the ‘predictability’ hypothesis are not supported in this study system.

Cold climates and the evolution of viviparity in reptiles: cold incubation temperatures produce poor-quality offspring in the lizard, Sceloporus virgatus

Abstract Evolutionary origins of viviparity among the squamate reptiles are strongly associated with cold climates, and cold environmental temperatures are thought to be an important selective force behind the transition from egg-laying to live-bearing. In particular, the low nest temperatures associated with cold climate habitats are thought to be detrimental to the developing embryos or hatchlings of oviparous squamates, providing a selective advantage for the retention of developing eggs in utero , where the mother can provide warmer incubation temperatures for her eggs (by actively thermoregulating) than they would experience in a nest. However, it is not entirely clear what detrimental effects cold incubation temperatures may have on eggs and hatchlings, and what role these effects may play in favouring the evolution of viviparity. Previous workers have suggested that viviparity may be favoured in cold climates because cold incubation temperatures slow embryogenesis and delay hatching of the eggs, or because cold nest temperatures are lethal to developing eggs and reduce hatching success. However, incubation temperature has also been shown to have other, potentially long-term, effects on hatchling phenotypes, suggesting that cold climates may favour viviparity because cold incubation temperatures produce offspring of poor quality or low fitness. We experimentally incubated eggs of the oviparous phrynosomatid lizard, Sceloporus virgatus , at temperatures simulating nests in a warm (low elevation) habitat, as is typical for this species, and nests in a colder (high elevation) habitat, to determine the effects of cold incubation temperatures on embryonic development and hatchling phenotypes. Incubation at cold nest temperatures slowed embryonic development and reduced hatching success, but also affected many aspects of the hatchlings» phenotypes. Overall, the directions of these plastic responses indicated that cold-incubated hatchlings did indeed exhibit poorer quality phenotypes; they were smaller at hatching (in body length) and at 20 days of age (in length and mass), grew more slowly (in length and mass), had lower survival rates, and showed greater fluctuating asymmetry than their conspecifics that were incubated at warmer temperatures. Our findings suggest that cold nest temperatures are detrimental to S. virgatus , by delaying hatching of their eggs, reducing their hatching success, and by producing poorer quality offspring. These negative effects would likely provide a selective advantage for any mechanism through which these lizards could maintain warmer incubation temperatures in cold climates, including the evolution of prolonged egg retention and viviparity.

The Effects of Reproductive Mode and Climate on Reproductive Success in the Australian Lizard, Lerista bougainvillii

The most widely accepted hypothesis invokes climates as the selective force respon- sible for the evolution of viviparity in reptiles. The hypothesis proposes that viviparity is adaptive in climates because developing embryos experience warmer temperatures in utero (through maternal thermoregulation) than they would in a nest. Most authors have assumed that these warmer in- cubation temperatures provide an advantage by protecting embryos from lethally low temperatures or by allowing them to hatch before the onset of winter. Thus, the hypothesis (at least in its tra- ditional form) purports that viviparity evolves in climates because females that retain their develop- ing offspring in utero will have greater reproductive success than females that lay their eggs in a nest. To test this hypothesis, I conducted a reciprocal transplant experiment using the reproductively bimodal Aus- tralian lizard, Lerista bougainvillii. Gravid oviparous and viviparous females were transplanted into field enclosures in both a and a cold climate, to monitor the effects of climate on their reproductive success. The live-bearers had higher reproductive success than the egg-layers in both climates, but repro- ductive success did not differ between the hot and climates within either reproductive mode. The viviparous lizards were more successful at producing offspring, regardless of climatic conditions. Thus, viviparity provided an advantage (in terms of embryo and/or neonate survival) under the conditions of the experiment, but this advantage was not restricted to environments.

Intraspecific Variation in Reproductive Mode within the Scincid Lizard Saiphos equalis

Although viviparity (live-bearing) has evolved from oviparity (egg-laying) more frequently in squamate reptiles than in any other vertebrate lineage, there are few well-documented cases of taxa that either (i) exhibit a ‘transitional’ reproductive state (i.e. with a reproductive mode intermediate between ‘normal’ oviparity and viviparity) or (ii) contain both oviparous and viviparous populations within the same species. Although rare, such taxa offer exceptional opportunities to test hypotheses concerning the evolution of viviparity in reptiles. Our data show that the scincid lizard Saiphos equalis displays both of the characteristics listed above. These small semi-fossorial skinks from south-eastern Australia exhibit geographic variation in reproductive mode, and some populations show an ‘intermediate’ mode. We examined the reproductive mode of Saiphos equalis over the geographic range of the species using preserved museum specimens, and we gathered detailed information on reproductive output of captive lizards collected from a high-elevation site (Riamukka, in the northern highlands of New South Wales) and from a coastal area (Sydney, southern New South Wales). Lizards from Riamukka were viviparous (i.e. they produced fully formed young enclosed in membranous sacs), whereas Sydney lizards produced incompletely developed embryos inside partially calcified eggshells. Incubation periods of the eggs from Sydney lizards were very brief (5.5 1.7 days v. >35 days in sympatric oviparous skinks), indicating that oviparous S. equalis represent a true evolutionary intermediate between ‘normal’ oviparity and viviparity.

A New Hypothesis for the Evolution of Viviparity in Reptiles

Viviparity has evolved many times within squamate reptiles, mostly in cool climates, but the selective advantages of uterine retention of eggs remain obscure. Previous analyses have assumed that intrauterine incubation enhances offspring survival because of early hatching or protection of the young in utero. I suggest instead that prolonged uterine retention directly enhances hatchling viability, because eggs incubated at maternal body temperatures produce better hatchlings than do eggs incubated at normal nest temperatures. To test this idea, I incubated eggs of two species of montane scincid lizards from southeastern Australia (Bassiana duperreyi and Nannoscincus maccoyi) under thermal regimes designed to simulate temperatures in nests and maternal oviducts. Hatchling phenotypes were substantially affected by incubation temperatures. The variables affected by incubation at maternal versus nest thermal regimes include the hatchling's morphology (body size, relative tail length), running speed in a labo...

Étude comparative de la membrane coquillère chez les souches ovipare et vivipare du lézard Lacerta vivipara

Evolution of viviparity in reptiles has resulted in more or less complete regression of the eggshell membrane. Such a regression has been studied in a lizard, Lacerta vivipara, which has both oviparous and viviparous populations. In oviparous reproduction, eggs laid have parchmentlike eggshells with a mean thickness of 36 μm. These eggshell membranes are composed of fibrils and of calcite, which is distributed over the outer surface and in the interfibrillar matrix. In viviparous reproduction, a transparent eggshell membrane remains between the embryonic and maternal tissues throughout pregnancy. This membrane consists mainly of fibrils and has only minor traces of calcite. Its mean thickness is only 9 μm. Reduction of thickness and of calcification is thought to be an adaptation that allows better respiratory exchanges at the end of pregnancy, when embryos require more oxygen. The author emphasizes that species with bimodality of reproduction (oviparity and viviparity) are of considerable interest in research investigating the evolution of viviparity in reptiles.

The Evolution of Viviparity in Amniote Vertebrates: Egg Retention Versus Egg Size Reduction

We critically examine a recent explanation for the absence of viviparity in birds that depends heavily on a model that was developed to account for viviparity in squamate reptiles. We propose that the elevated body temperature of birds precludes extended egg retention, presumably an early stage in the evolution of viviparity from an oviparous ancestor, probably through constraints on the rate of oxygen transfer to developing embryos. We demonstrate that if the effects of endothermy are included in the model developed to account for the evolution of viviparity in reptiles, then qualitative and quantitative differences in embryonic developmental rates are predicted between reptiles and birds as a result of eggs being retained within the uterine environment. Our modification of the model thus offers an explanation for the total absence of viviparity in birds. We propose that the evolutionary sequence for mammalian viviparity from an endothermic oviparous ancestor was through the progressive production of smaller eggs, with proportionally shorter embryonic developmental times, which would allow for relatively longer periods of egg retention before oxygen-supply constraints would be reached. The critical characteristic allowing extensive egg size reduction in the mammals was lactation, which allowed the feeding of tiny altricial neonates. The absence of lactation, or some analogous method of feeding very small young, has constrained birds from following the evolutionary pathway to viviparity that we propose for mammals.

The evolution of viviparity in reptiles: A physiological model and its ecological consequences

Viviparity has evolved almost 100 times among lizards and snakes. Most scientific interest in this phenomenon has focussed on environmental variables that may have stimulated the evolution of viviparity via intermediate stages of prolonged oviductal retention of eggs (egg retention, or ER). Little attention has been paid to more proximate questions (e.g. what endocrine mechanisms control the duration of ER?) and their evolutionary consequences (e.g. is the degree of ER in a given female fixed or labile? Are there specific features of endocrine control systems for ER which may preadapt a taxon to the evolution of viviparity?). We develop a recently-proposed physiological model for prolonged uterine retention of eggs (Guillette, 1985), and investigate its implications for the evolution of reptilian viviparity. Our model is unusual in combining proximate mechanisms with ultimate (evolutionary) processes. We suggest that the duration of ER is controlled by circulating levels of progesterone, and that progesterone secretion by the adrenals in response to environmental cues may prolong ER. Hence, there may be a large phenotypic component to variance in ER. This mechanism may facilitate the evolution of viviparity in some taxa and in some habitats, by increasing variance in ER and hence (1) expediting the rate of change in ER inducible by selection, and (2) overcoming the necessity for very brief ER to confer a selective advantage. In situations in which prolonged ER confers a higher fitness to the reproducing organism, this character may evolve through genetic assimilation (“fixing” of a phenotypic response, from facultative to obligate). Our model generates several testable predictions, in terms of both endocrine mechanisms and evolutionary pathways.