The geography of snake reproductive mode: a global analysis of the evolution of snake viviparity

Abstract

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. ResultsWe 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 conclusionsWe 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.

Habits and characteristics of arboreal snakes worldwide: arboreality constrains body size but does not affect lineage diversification

“…Parity mode for arboreal snakes parallels what is found across snakes generally, with ~21% of arboreal snakes categorized as viviparous here (Table 3); this is comparable to a recent study on the reproductive modes of non-marine/non-scolecophidian snakes globally (21.5% of snakes are viviparous globally; Feldman et al, 2015).…”

Viviparity does not affect the numbers and sizes of reptile offspring

“…Griffith, Brandley, Belov, & Thompson, ; Van Dyke, Brandley, & Thompson, ). Also, live‐bearers tend to live in different climatic zones than do their oviparous relatives (Feldman et al, ; Shine, ), and generally produce only a single litter per year, whereas multiple‐clutching is frequent in egg‐layers (Meiri et al, ; Shine, ). Given the breadth of these changes, we might also expect other reproductive traits (such as the sizes and numbers of offspring) to shift.…”

“…In most cases, the transition has been from oviparity to viviparity rather than the reverse (Blackburn, ; Griffith et al, ; Wright, Lyons, Brandley, & Hillis, , but see Lynch & Wagner, ; Pyron & Burbrink, ). This shift has likely happened as oviparous lineages have penetrated cooler climatic conditions (Feldman et al, ; Shine, , ). In such areas, the ability of gravid females to maintain high body temperatures (via behavioural thermoregulation) may keep their uterine offspring warm and thereby enhance offspring viability relative to embryos deposited in (cool) external nests (Shine, , ).…”

Hypoxia and hypothermia as rival agents of selection driving the evolution of viviparity in lizards

“…Therefore, emerging theory predicts that the evolution of reptilian viviparity accelerates diversification rates by facilitating access to the ecological opportunity offered by otherwise inaccessible coldclimate environments (Pincheira-Donoso, Tregenza, et al, 2013). However, although this prediction has been supported by comparative evidence (Hodges, 2004;Shine, 2005;Pincheira-Donoso, Tregenza, et al, 2013;Pyron & Burbrink, 2014), this 'cold-climate' or 'hypothermia' hypothesis ignores the multiple other climatic factors that vary geographically and covary with thermal gradients (Lambert & Wiens, 2013;Feldman et al, 2015). Consequently, the role of temperature as the primary driving force behind transitions to viviparity may have spuriously been overestimated, eclipsing the role of other sources of selection.…”