A global test of the cold‐climate hypothesis for the evolution of viviparity of squamate reptiles

Abstract

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.

Sex determination systems in reptiles are related to ambient temperature but not to the level of climatic fluctuation

“…We propose that selection has acted so that non-avian reptile species reproduce preferentially during the warmer and less variable months of the year with strong selection acting on the length of breeding seasons depending on the biogeographical distribution of the species. Third, our data confirm that viviparous species are strongly associated with GSD [32] and their distributions are limited to cold areas [31]. Four, we found a correlation with precipitation that is conditioned by reproductive mode.…”

“…Viviparous species are more likely to have GSD [32] and are also more likely to live in colder areas than oviparous ones [31]; a pattern we recapitulated in this study with 30 out of 31 viviparous species having GSD and a preference for colder climates (PGLS, P < 0.0001, slope = − 6.25, alpha = 14.9, n = 213 species; Additional file 1: Figure S1). To verify whether viviparity influenced the results, we constrained the analysis to oviparous species only.…”

“…Moreover, the empirical association between specific climatic conditions and sex determination systems is also supported by data from viviparous reptiles. These reptile species inhabit extremely cold regions [31] and are strongly associated with GSD [32]. However, a study on the association of sex determination systems, environmental factors, breeding season lengths, and life-history traits has not been conducted across a wide range of taxa.…”

Climatic niche evolution in the viviparousSceloporus torquatusgroup (Squamata: Phrynosomatidae)

“…Viviparity among squamate reptiles (lizards and snakes) has evolved from oviparity approximately 100 times (Blackburn, 2000, 2015) and has been a model system for testing many evolutionary hypotheses regarding the origin of viviparity in vertebrates (Lambert & Wiens, 2013). In this regard, viviparity among reptiles has been linked to cold climates as it provides a selective advantage that prevents the death of embryos in nests owing to low temperatures (Tinkle & Gibbons, 1977; Shine, 1985; Lambert & Wiens, 2013; Ma et al, 2018). Moreover, evidence suggests that certain lizard species that have evolved viviparity remain adaptively constrained to cold climates (Pincheira-Donoso et al, 2013).…”

Peer Review #1 of "Climatic niche evolution in the viviparous Sceloporus torquatus group (Squamata: Phrynosomatidae) (v0.1)"

“…Viviparity among squamate reptiles (lizards and snakes) has evolved from oviparity approximately 100 times (Blackburn, 2000(Blackburn, , 2015 and has been a model system for testing many evolutionary hypotheses regarding the origin of viviparity in vertebrates (Lambert & Wiens, 2013). In this regard, viviparity among reptiles has been linked to cold climates as it provides a selective advantage that prevents the death of embryos in nests owing to low temperatures (Tinkle & Gibbons, 1977;Shine, 1985;Lambert & Wiens, 2013;Ma et al, 2018).…”