It is of fundamental importance for the field of evolutionary biology to understand when and why major evolutionary transitions occur. Live‐bearing young (viviparity) is a major evolutionary change ...and has evolved from egg‐laying (oviparity) independently in many vertebrate lineages and most abundantly in lizards and snakes. Although contemporary viviparous squamate species generally occupy cold climatic regions across the globe, it is not known whether viviparity evolved as a response to cold climate in the first place. Here, we used available published time‐calibrated squamate phylogenies and parity data on 3,498 taxa. We compared the accumulation of transitions from oviparity to viviparity relative to background diversification and a simulated binary trait. Extracting the date of each transition in the phylogenies and informed by 65 my of global palaeoclimatic data, we tested the nonexclusive hypotheses that viviparity evolved under the following: (a) cold, (b) long‐term stable climatic conditions and (c) with background diversification rate. We show that stable and long‐lasting cold climatic conditions are correlated with transitions to viviparity across squamates. This correlation of parity mode and palaeoclimate is mirrored by background diversification in squamates, and simulations of a binary trait also showed a similar association with palaeoclimate, meaning that trait evolution cannot be separated from squamate lineage diversification. We suggest that parity mode transitions depend on environmental and intrinsic effects and that background diversification rate may be a factor in trait diversification more generally.
Frequency of transitions from oviparity to viviparity and palaeoclimate. (a) Empirically estimated transitions from oviparity to viviparity in squamates (dark grey) and the ratio of oxygen isotope (δ18O) as proxy for global mean temperature (light grey) are displayed per million years from 65 million years ago to present. Temperature (y‐axis) and number of transitions (z‐axis) are shown as smoothed lines (spanλ = 0.25).
Aim: The evolution of viviparity in squamate reptiles has attracted considerable scientific attention since the beginning of last century. The cold-climate hypothesis posits that cold regions favor ...viviparity (and therefore the incidence of viviparous squamates is increased in these regions) because viviparous females can use thermoregulatory behavior to shorten embryonic developmental time and to reduce exposure of embryos to stressful temperatures. However, a rigorous global-scale test of the impact of viviparity on the developmental time and viability of embryos is still absent. Recently developed biophysical models and climate databases enable us to conduct a mechanistic test of this hypothesis. Location: Global. Time period: Summer. Major taxa studied: Squamata. Methods: We integrated global climate data, a biophysical model, and developmental functions to quantify the effects of temperature on embryo developmental time, developmental viability, and energy consumption of oviparous versus viviparous embryos. To examine the accuracy of our predictions, we calculated the percentage of squamate reptiles that were viviparous in each region and assessed developmental temperature of gravid females, latitude and elevation as predictors for the percentage of squamate reptiles. Results: Compared with oviparous embryos, viviparous embryos develop faster in cold regions, and experience similar embryonic developmental viability. Across most latitudes and elevations, the total energetic cost of development is lower for viviparous embryos than for oviparous embryos. Cold regions contain a higher proportion of viviparous species than do hot regions. By comparing the distribution pattern of viviparity and temperature effects on embryonic development, we found that shortened development time provided the strongest benefit of viviparity. Main conclusions: Our global and biophysical model based comparison generally supports the cold-climate hypothesis. Moreover, viviparity in cold climates appears beneficial primarily by shortening developmental time.
Viviparity, the bearing of live young, has evolved well over 100 times among squamate reptiles. This reproductive strategy is hypothesized to allow maternal control of the foetus' thermal environment ...and thereby to increase the fitness of the parents and offspring. Two hypotheses have been posited to explain this phenomenon: (i) the cold‐climate hypothesis (CCH), which advocates low temperatures as the primary selective force; and (ii) the maternal manipulation hypothesis (MMH), which advocates temperature variability as the primary selective force. Here, we investigate whether climatic and geographic variables associated with the CCH vs. the MMH best explain the current geographical distributions of viviparity in lizards while incorporating recent advances in comparative methods, squamate phylogenetics and geospatial analysis. To do this, we compared nonphylogenetic and phylogenetic models predicting viviparity based on point‐of‐capture data from 20 994 museum specimens representing 215 lizard species in conjunction with spatially explicit bioclimatic and geographic (elevation and latitude) data layers. The database we analysed emphasized Nearctic lizards from three species‐rich genera (Phrynosoma, Plestiodon and Sceloporus); however, we additionally analysed a less substantial, but worldwide sample of species to verify the universality of our Nearctic results. We found that maximum temperature of the warmest month (and, less commonly, elevation and maximum temperature of the driest quarter) was frequently the best predictor of viviparity and showed an association consistent with the CCH. Our results strongly favour the CCH over the MMH in explaining lizard reproductive mode evolution.
Evolutionary transitions in life‐history strategies, such as the shift from egg‐laying to live birth (viviparity) are of great interest to evolutionary biologists. In squamate reptiles, several ...hypotheses have been proposed to explain viviparity including the cold climate hypothesis, maternal manipulation hypothesis, hypoxia hypothesis, and several others. We used two approaches: first we studied 45 species of Liolaemus, a genus where nearly 50% of species are viviparous, using a diverse ecophysiological dataset to examine the cold climate and maternal manipulation hypotheses. We collected environmental thermal data (accounting for elevational differences among species), physiological traits including preferred body temperature and its coefficient of variation as an indicator of precision in thermoregulation. Additionally, we collected standard metabolic rates for 23 of the 45 species. In one clade (the darwinii group of species) with both reproductive modes, we ran our second approach. We tested for differences in thermal physiology and metabolic rates between viviparous and oviparous species during pregnancy and non‐pregnancy periods. The cold climate hypothesis received strong support because viviparous species occur in sites with colder air temperatures (including areas at both higher elevations and latitudes) compared with oviparous species. Our detailed analysis showed that the maternal manipulation hypothesis also is supported; pregnant viviparous females show lower variation in their selected temperature. Our evidence suggests that the Andean orogeny is likely to have played a key role in the diversification of Liolaemus lizards and the evolution of viviparity in this clade may have been driven by a variety of physiological advantages accrued at different stages of embryogenesis and over evolutionary time. Thus, historical climate changes may have led to egg retention and may have been accompanied by other adaptations such as thermoregulation precision.
Several hypotheses have been proposed to explain viviparity in Reptiles including the cold climate hypothesis, maternal manipulation hypothesis, hypoxia hypothesis, and several others. We collected environmental thermal data, preferred body temperature, its coefficient of variation (as an indicator of precision in thermoregulation) and standard metabolic rates for several species of Liolaemus. We tested for differences in thermal physiology and metabolic rates between viviparous and oviparous species during pregnancy and non‐pregnancy periods. Both, the cold climate and the maternal manipulation hypotheses were supported. Viviparous species occur in sites with colder air temperatures and pregnant viviparous females show lower variation in their selected temperature than oviparous gravid females. Historical climate changes may have led to egg retention and may have been accompanied by other adaptations such as thermoregulation precision.
AIM: Although most reptiles are oviparous, viviparity is a common mode of reproduction in squamates and has evolved multiple times in different lineages. We test two prevailing hypotheses regarding ...the biogeography of reptile reproductive modes to evaluate the selective forces driving the evolution of viviparity in snakes. The cold climate hypothesis posits that viviparity is selected for in cold climates, whereas the climatic predictability hypothesis predicts that viviparity is advantageous in seasonal climates. LOCATION: Global. METHODS: We collated detailed distribution maps and reproductive mode data for 2663 species of the world's terrestrial alethinophidian snakes. We studied the relationship between snake reproductive mode and environmental predictors. We applied both an ecological and an evolutionary approach to study snake reproductive mode by performing the analyses at the assemblage level and species level, respectively. We analysed our data at the global and continental scales to learn whether tendencies to viviparity are similar world‐wide. RESULTS: We found strong support for the cold climate hypothesis and the assumption that viviparity is an adaptation to cold environments. There was little support for the climatic predictability hypothesis. Nonetheless, viviparous species are not restricted to cold environments. MAIN CONCLUSIONS: We conclude that viviparity is adaptive in cold climates, but not necessarily in unpredictable/seasonal climates. Current distributions may not reflect the climate at the time and place of speciation. We suspect many viviparous snakes inhabiting warm climates are members of lineages that originated in colder regions, and their occurrence in maladaptive environments is a result of phylogenetic conservatism.
Parity mode (oviparity/viviparity) importantly affects the ecology, morphology, physiology, biogeography and evolution of organisms. The main hypotheses explaining the evolution and maintenance of ...viviparity are based on bioclimatic predictions and also state that the benefits of viviparity arise during the reproductive period. We identify the main climatic variables discriminating between viviparous and oviparous Eurasian common lizard (Zootoca vivipara) occurrence records during the reproductive period and over the entire year.
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
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
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Cold environmental temperature is detrimental to reproduction by oviparous squamate reptiles by prolonging incubation period, negatively affecting embryonic developmental processes, and by killing ...embryos in eggs directly. Because low soil temperature may prevent successful development of embryos in eggs in nests, the geographic distributions of oviparous species may be influenced by the thermal requirements of embryos. In the present study, we tested the hypothesis that low incubation temperature determines the northern distributional limit of the oviparous lizard Sceloporus undulatus. To compare the effects of incubation temperature on incubation length, egg and hatchling survival, and hatchling phenotypic traits, we incubated eggs of S. undulatus under temperature treatments that simulated the thermal environment that eggs would experience if located in nests within their geographic range at 37°N and north of the species' present geographic range at latitudes of 44 and 42°N. After hatching, snout-vent length (SVL), mass, tail length, body condition (SVL relative to mass), locomotor performance, and growth rate were measured for each hatchling. Hatchlings were released at a field site to evaluate growth and survival under natural conditions. Incubation at temperatures simulating those of nests at 44°N prolonged incubation and resulted in hatchlings with shorter SVL relative to mass, shorter tails, shorter hind limb span, slower growth, and lower survival than hatchlings from eggs incubated at temperatures simulating those of nests at 37 and 42°N. We also evaluated the association between environmental temperature and the northern distribution of S. undulatus. We predicted that the northernmost distributional limit of S. undulatus would be associated with locations that provide the minimum heat sum (~495 degree-days) required to complete embryonic development. Based on air and soil temperatures, the predicted northern latitudinal limit of S. undulatus would lie at ~40.5-41.5°N. Our predicted value closely corresponds to the observed latitudinal limit in the eastern United States of ~40°N. Our results suggest that soil temperatures at northern latitudes are not warm enough for a sufficient length of time to permit successful incubation of S. undulatus embryos. These results are consistent with the hypothesis that incubation temperature is an important factor limiting the geographic distributions of oviparous reptile species at high latitudes and elevations.
Females of several lizard species modify their body temperature during pregnancy, probably in connection with the optimisation of hatchling phenotypes. We studied variations in the temperature ...selected by gravid females compared with those selected by males and non-gravid females in an oviparous population of
Zootoca vivipara (Jacquin, 1797) (Squamata: Lacertidae) of Northern Spain and examined the effects of incubation temperature on the phenotypic variation of hatchlings. Cloacal temperatures of gravid females active in the field were lower than those of males and non-gravid females, as well as the temperatures selected in a thermal gradient created in the laboratory (mean±s.d.: 32.33±1.27
°C for gravid females; 34.05±1.07
°C for males and non-gravid females). Effects of temperature were assessed by incubating eggs at five constant temperatures (21, 25, 29, 32 and 34
°C). Incubation time decreased as temperature increased, following a negative exponential function. Incubation temperatures also affected the hatchlings’ morphology: hatchlings incubated at 34
°C had shorter heads than those from other temperatures. Survival at 34
°C (58%) was significantly lower than at the other temperatures (mean 93%). Pregnant females select lower body temperature, approaching the temperatures that optimise hatchling phenotypes, according to predictions of the maternal manipulation hypothesis on the evolution of viviparity. The shift in preferred temperature by pregnant females would result in only a very short delay, if any, of hatching time and, because the temperature selected by pregnant females is much higher than average temperatures recorded in natural nests of
Z. vivipara, egg retention considerably shortens incubation time, according to predictions of the cold-climate hypothesis. Our experimental results indicate that the two main hypotheses on the evolution of viviparity are compatible in our study model.
Each year, as the warmth of summer turns into the cool of autumn and the cold of winter, snakes disappear from the Canadian landscape. For several months of the year, winter weather at high latitudes ...is much too cold for snakes to be active in the open and they must seek subterranean shelter to hibernate. This long period underground is one during which these animals are subject not only to the possibility of mortality, but also to lost opportunity for activities such as foraging and the acquisition of resources for reproduction. Winter is thus a major constraint on the life histories of temperate-zone snakes. Short, cool summers further restrict their foraging and reproductive opportunities. In apparent response to this challenge, most high-latitude snake species are viviparous, counter to what is seen in warmer climes. Viviparity allows gravid females to “manipulate” the developmental temperature of their progeny, via behavioral thermoregulation, until those offspring are independent, an option not open to oviparous species. However, viviparity also has costs, not least of which is a pronounced reduction in feeding during pregnancy, which means that the post-partum female has only a short time before winter to make up the reserves (“capital”) that she spent on reproduction and will need for future reproduction; therefore, reproduction in consecutive years is not always possible. Evidently, the demographic costs of viviparity are outweighed by its advantages, but what remains unexplained is how some oviparous species manage to persist at high latitudes. Demographic advantages of oviparous over viviparous species, due to shorter “pregnancy” of the former, are not apparent from limited temperate-zone studies. More likely, cool-climate oviparous species also reproduce successfully by taking advantage of the thermal heterogeneity of the environment, especially by thermoregulating precisely while gravid and/or by careful selection of nest sites.
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