Thermal melanism explains macroevolutionary variation of dorsal pigmentation in Eurasian vipers

Abstract

Colouration may endorse thermoregulatory and antipredatory functions in snakes. The thermal melanism hypothesis predicts that dark-coloured individuals are ecologically favoured in cool climates. However, the loss of aposematic and cryptic colourations may imply high predation for melanistic snakes. Here, we used the monophyletic group of Eurasian vipers (subfamily Viperinae) to test whether an increase in the extent of dark area inside the characteristic zigzag dorsal pattern is associated to colder environments. We measured two colouration traits in zigzag-patterned individuals (number of dorsal marks and weighted pigmentation index) and used a phylogenetic comparative approach to explore macroevolutionary patterns of dorsal pigmentation and test whether its extent is associated to ecogeographic characteristics of lineages’ ranges. Phylogenetically-naïve and phylogenetically-informed analyses yielded a significant association between the degree of pigmentation of the zigzag pattern and environmental variables such as solar radiation, elevation and latitude. The degree of pigmentation of the zigzag pattern is highlighted as an adaptive trait that matches range attributes mirroring cold environments irrespective of the phylogeny. These results constitute the first large-scale evidence supporting the thermal melanism hypothesis in snakes, opening new avenues of inquiry for the mechanisms that shape the evolution of colour phenotypes.

Substrate thermal properties influence ventral brightness evolution in ectotherms

“…Darker integuments may contribute not only to better camouflage, but also to thermoregulatory functions in colder environments (e.g., allowing the brain to reach optimal temperatures faster 46 ) and UV protection (e.g., protecting the animal from higher radiations at higher altitudes 47 ). The present results are further supported by Martínez-Freiría et al 48 who found that darker dorsal colors in European vipers are associated with cold environments. Overall, our findings on the dorsal and ventral brightness suggest that these body regions are subjected to divergent selective forces.…”

Rapid ecological and evolutionary divergence during a poleward range expansion

“…Contrary to our expectation, given the fact that many ectothermic animals (i.e. reptiles, insects) show darker coloration at northern latitudes (Watt, 1968;Guppy, 1986;Svensson & Waller, 2013;Martínez-Freiría et al, 2020), we did not find darker opisthosoma pigmentation with increasing latitude. However, we did find a significant association of pigmentation with one environmental principal component (PC4).…”

Integrative taxonomy reveals two species and intraspecific differentiation in theVipera latastei–monticolacomplex

“…Regarding morphological variability, marked differences occurred in biometric, scalation and dorsal coloration traits, particularly between species and among V. monticola subspecies. Several studies addressing morphological variability in Vipera species highlighted the adaptive and plastic character of several morphological traits, as they were found varying in accordance to environmental gradients (e.g., Martínez-Freiría et al, 2009;Martínez-Freiría, Toyama, et al, 2020;Santos et al, 2014). As in previous studies using ecological modeling tools (Brito et al, 2008;Freitas et al, 2018;Santos et al, 2006), we found that V. monticola occurs across a narrower topo-climatic niche than V. latastei (Data S4), which makes the former more sensitive to extreme and stochastic changes than the later.…”

“…monticola subspecies. Several studies addressing morphological variability in Vipera species highlighted the adaptive and plastic character of several morphological traits, as they were found varying in accordance to environmental gradients (e.g., Martínez‐Freiría & Brito, 2013; Martínez‐Freiría et al, 2009; Martínez‐Freiría, Toyama, et al, 2020; Santos et al, 2014). As in previous studies using ecological modeling tools (Brito et al, 2008; Freitas et al, 2018; Santos et al, 2006), we found that V .…”