Evolution of Viviparity: A Phylogenetic Test of the Cold-Climate Hypothesis in Phrynosomatid Lizards

Abstract

The evolution of viviparity is a key life-history transition in vertebrates, but the selective forces favoring its evolution are not fully understood. With >100 origins of viviparity, squamate reptiles (lizards and snakes) are ideal for addressing this issue. Some evidence from field and laboratory studies supports the "cold-climate" hypothesis, wherein viviparity provides an advantage in cold environments by allowing mothers to maintain higher temperatures for developing embryos. Surprisingly, the cold-climate hypothesis has not been tested using both climatic data and phylogenetic comparative methods. Here, we investigate the evolution of viviparity in the lizard family Phrynosomatidae using GIS-based environmental data, an extensive phylogeny (117 species), and recently developed comparative methods. We find significant relationships between viviparity and lower temperatures during the warmest (egg-laying) season, strongly supporting the cold-climate hypothesis. Remarkably, we also find that viviparity tends to evolve more frequently at tropical latitudes, despite its association with cooler climates. Our results help explain this and two related patterns that seemingly contradict the cold-climate hypothesis: the presence of viviparous species restricted to lowelevation tropical regions and the paucity of viviparous species at high latitudes. Finally, we examine whether viviparous taxa may be at higher risk of extinction from anthropogenic climate change. K E Y W O R D S :Climate, comparative methods, life-history evolution, phylogeny, reproductive mode, squamates.The transition from oviparity (egg laying) to viviparity (live bearing) is a major evolutionary shift in life history with many potential consequences for the morphology, physiology, behavior, and ecology of an organism (Shine and Bull

Repeated evolution of viviparity in phrynosomatid lizards constrained interspecific diversification in some life-history traits

“…The evolution of viviparity in reptiles increased morphological and lineage diversification [7,8,10]. Our study found the opposite pattern: viviparous species exhibited reduced rates of evolution and lower diversification in some life-history traits.…”

“…Viviparity has likely evolved independently six times within this North American family [7]. We predicted higher diversification rates in the life histories of viviparous species.…”

“…With the exception of clutch/ litter size, data were not available for all 61 species (we show sample sizes in table 1). We combined these data with a timecalibrated phylogeny [12] and ancestral estimates of oviparity/ viviparity [7]. Our dataset included representative species from five of the six independent origins of viviparity in the family (electronic supplementary material, figure S1).…”

“…For example, toe pads in Anolis lizards [2], pharyngeal jaws in cichlid fishes [3] and antifreeze glycoproteins in notothenioid fishes of Antarctica [4] have all been described as key innovations leading to increased phenotypic diversification and higher rates of speciation as animals colonized a wider array of ecological niches. In lizards and snakes, viviparity has evolved independently more than 100 times [5] and may be a key innovation that allowed females to maximize offspring fitness in cold environments [6][7][8]. In addition, the ability of viviparous females to actively thermoregulate during pregnancy allows them to manipulate the phenotype of their offspring as well as to reduce the variance in the temperature experienced by developing embryos [9].…”

“…Recent studies have suggested that the evolution of viviparity in reptiles increased lineage diversification [7,8]. Oufiero & Gartner [10] demonstrated that viviparous lizards of the North American family Phrynosomatidae experienced higher evolutionary rates leading to greater interspecific diversification in morphological traits such as pelvic height and width, humerus length and radius length compared with oviparous species of the same family.…”