Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards

Abstract

Viviparity, an innovation enhancing maternal control over developing embryos, has evolved >150 times in vertebrates, and has been proposed as an adaptation to inhabit cold habitats. Yet, the behavioral, physiological, morphological, and life history features associated with live-bearing remain unclear. Here, we capitalize on repeated origins of viviparity in phrynosomatid lizards to tease apart the phenotypic patterns associated with this innovation. Using data from 125 species and phylogenetic approaches, we find that viviparous phrynosomatids repeatedly evolved a more cool-adjusted thermal physiology than their oviparous relatives. Through precise thermoregulatory behavior viviparous phrynosomatids are cool-adjusted even in warm environments, and oviparous phrynosomatids warm-adjusted even in cool environments. Convergent behavioral shifts in viviparous species reduce energetic demand during activity, which may help offset the costs of protracted gestation. Whereas dam and offspring body size are similar among both parity modes, annual fecundity repeatedly decreases in viviparous lineages. Thus, viviparity is associated with a lower energetic allocation into production. Together, our results indicate that oviparity and viviparity are on opposing ends of the fast-slow life history continuum in both warm and cool environments. In this sense, the ‘cold climate hypothesis’ fits into a broader range of energetic/life history trade-offs that influence transitions to viviparity.

Reproductive pattern of the southern bunchgrass lizard (Sceloporus aeneus) from Cuautepec de Hinojosa, Hidalgo, Mexico

“…Therefore, regardless of parity mode, species of similar size will reach maturity at the same age (Domínguez-Guerrero et al, 2022).…”

Reproductive traits and change in body shape of neonates in the Oak Forest Skink, Plestiodon lynxe

“…Unlike oviparous species, viviparous species are prevalent in cold environments where the risk of predation is relatively low, favouring the acquisition of a lower metabolic rate and lower reproductive allotment (Auer et al, 2018). On the other hand, Domínguez‐Guerrero et al (2022) showed that in phrynosomatid lizards, transitions from oviparity to viviparity were associated with a reduction in body temperature of 5°C and consequently with a lower metabolic rate and lower specific mass production.…”

Viviparity imparts a macroevolutionary signature of ecological opportunity in Liolaemus lizards

“…For example, viviparous ray-finned fishes (Cyprinodontiformes), and cartilaginous fishes (Chondrichthyes), exhibit higher rates of diversification than their oviparous relatives, a product of their ability to colonize new ecological spaces 21,108 . Further, larger sizes in viviparous species than oviparous relatives is observed in other lineages, including spiny lizards, sharks and rays 3,21 . Together, this study supports the notion that evolution of viviparity opens the opportunity to colonize new habitats and exploit available resources: these features together prompt faster rates of phenotypic diversification and the evolution of larger body sizes, shedding new light on the mechanisms underpinning the high diversity of viviparous species in the most extreme thermal habitats in the world.…”

“…Colonization of cold habitats by viviparous ectotherms (such as Liolaemus) depends on the ability of individuals to regulate their field body temperature within their preferred range (i.e., thermoregulatory behavior) and maximize their performance and fitness 3,73 . Indeed, behavioral thermoregulation in viviparous Liolaemus (which are mainly saxicolous 42 ) is more precise than oviparous species 73 .…”

“…Viviparity (live-bearing) is a major evolutionary innovation that affords enhanced maternal control over embryonic development, and drastically reshapes how organisms interact with their thermal habitat [1][2][3] . Through active thermoregulation, viviparous females control the incubation temperature for developing embryos, optimizing the neonate's phenotype and maximizing offspring survivorship [4][5][6] .…”