Reproductive mode evolution in lizards revisited: updated analyses examining geographic, climatic and phylogenetic effects support the cold-climate hypothesis

J Evol Biol. 2014 Dec;27(12):2767-80. doi: 10.1111/jeb.12536. Epub 2014 Nov 22.

Abstract

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.

Keywords: Phrynosoma; Plestiodon; Sceloporus; cold-climate hypothesis; high elevation; lizards; maternal manipulation hypothesis; oviparity; phylogeny; viviparity.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Biological Evolution*
  • Climate*
  • Cold Temperature*
  • Female
  • Geography
  • Lizards / physiology*
  • Models, Biological*
  • Phylogeny*
  • Species Specificity
  • United States
  • Viviparity, Nonmammalian / physiology*