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

Saúl F. Domínguez-Guerrero (), Fausto R. Méndez- de la Cruz, Norma L. Manríquez-Morán, Mark E. Olson, Patricia Galina-Tessaro, Diego M. Arenas-Moreno, Adán Bautista- del Moral, Adriana Benítez-Villaseñor, Héctor Gadsden, Rafael A. Lara-Reséndiz, Carlos A. Maciel-Mata, Francisco J. Muñoz-Nolasco, Rufino Santos-Bibiano, Jorge H. Valdez-Villavicencio, Guillermo A. Woolrich-Piña and Martha M. Muñoz
Additional contact information
Saúl F. Domínguez-Guerrero: Yale University
Fausto R. Méndez- de la Cruz: Universidad Nacional Autónoma de México
Norma L. Manríquez-Morán: Universidad Autónoma del Estado de Hidalgo
Mark E. Olson: Universidad Nacional Autónoma de México
Patricia Galina-Tessaro: Centro de Investigaciones Biológicas del Noroeste S. C.
Diego M. Arenas-Moreno: Universidad Nacional Autónoma de México
Adán Bautista- del Moral: Universidad Nacional Autónoma de México
Adriana Benítez-Villaseñor: Universidad Nacional Autónoma de México
Héctor Gadsden: Instituto de Ecología, A. C.
Rafael A. Lara-Reséndiz: Centro de Investigaciones Biológicas del Noroeste S. C.
Carlos A. Maciel-Mata: Universidad Autónoma del Estado de Hidalgo
Francisco J. Muñoz-Nolasco: Universidad Nacional Autónoma de México
Rufino Santos-Bibiano: Universidad Nacional Autónoma de México
Jorge H. Valdez-Villavicencio: Conservación de Fauna del Noroeste, A.C.
Guillermo A. Woolrich-Piña: Tecnológico Nacional de México campus Zacapoaxtla
Martha M. Muñoz: Yale University

Nature Communications, 2022, vol. 13, issue 1, 1-12

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-30535-w

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