Emergence of an evolutionary innovation: Gene expression differences associated with the transition between oviparity and viviparity

Abstract

Our understanding of the evolution of complex biological traits is greatly advanced by examining taxa with intermediate phenotypes. The transition from oviparity (egg‐laying) to viviparity (live‐bearing) has occurred independently in many animal lineages, but there are few phenotypic intermediates. The lizard Saiphos equalis exhibits bimodal reproduction, with some viviparous populations, and other oviparous populations with long egg‐retention, a rare trait where most of embryonic development occurs inside the mother prior to late ovipositioning. We posit that oviparous S. equalis represent an intermediate form between “true” oviparity and viviparity. We used transcriptomics to compare uterine gene expression in these two phenotypes, and provide a molecular model for the genetic control and evolution of reproductive mode. Many genes are differentially expressed throughout the reproductive cycle of both phenotypes, which have clearly different gene expression profiles overall. The differentially expressed genes within oviparous and viviparous individuals have broadly similar biological functions putatively important for sustaining embryos, including uterine remodelling, respiratory gas and water exchange, and immune regulation. These functional similarities indicate either that long egg‐retention is an exaptation for viviparity, or might reflect parallel evolution of similar gravidity‐related changes in gene expression in long egg‐retention oviparity. In contrast, gene expression changes across the reproductive cycle of long egg‐retaining oviparous S. equalis are dramatically different from those of “true” oviparous skinks (such as Lampropholis guichenoti), supporting our assertion that oviparous S. equalis exhibit an intermediate phenotype between “true” oviparity and viviparity.

Ecological and life‐history correlates of erythrocyte size and shape in Lepidosauria

“…Although not directly measured, it is inferred that viviparous species with placentation exchange respiratory gases and this is facilitated by changes in maternal blood chemistry that enhances oxygen exchange (Ingerman et al, 1991). To fully understand the link between oxygen demand, oxygen transport and reproductive mode, examples of within‐species (Rechnagel et al, 2021) and within‐individual variation (Laird et al, 2019), that is, showing both oviparous and viviparous reproductive modes, as well as cross‐species comparisons (Foster et al, 2020) all provide ideal opportunities to link evolutionary form to function. Our analysis suggests that changing blood oxygen‐carrying capacity by altering size and/or shape of erythrocytes is one mechanism to avoid constraints of low oxygen and may allow viviparous Lepidosauria to exploit higher altitude areas.…”

Australian lizards are outstanding models for reproductive biology research

“…In Australian lizards, evidence of obligate placentotrophy of organic nutrients is so far limited to skinks in the genera Carinascincus and Pseudemoia; candidate nutrient transporters in these taxa include lipoprotein lipase, and amino acidtransporting solute carriers (SLCs: Griffith et al 2013Griffith et al , 2016. Gene expression analyses, particularly transcriptomic studies, have identified thousands of genes that are likely to be involved in pregnancy in Australian lizards (Griffith et al 2016Hendrawan et al 2017;Foster et al 2020). These genes likely contribute to key pregnancy-related functions including uterine remodelling, nutrient and respiratory gas transport, and immune regulation, and testing the functions of these genes is the next step in understanding their role in the evolution of viviparity.…”

The evolution and physiology of male pregnancy in syngnathid fishes

“…The evolution of this type of reproductive complexity is currently of broad interest to evolutionary biologists (e.g. Van Dyke et al ., ; Griffith et al ., ; Pyron, ; Blackburn, ; Whittington et al ., ; Buddle et al ., ; Cornetti et al ., ; Gao et al ., ; Foster et al ., ).…”

“…Studies in a variety of vertebrates show that viviparous and oviparous parents exhibit differences in endocrine activity and metabolism, tissue remodelling and vascularity, nutrient provisioning, immune function, behaviour and performance, and regulation of gene expression (e.g. Qualls & Shine, ; Heulin et al ., , ; Adams et al ., ; Murphy & Thompson, ; Callard et al ., ; Whittington et al ., ; Griffith et al ., ; Foster et al ., ). These differences make parity mode a compelling subject for studies of comparative physiology, evolutionary biology, and the genetic basis of novel phenotypes.…”