Understanding the evolution of viviparity using intraspecific variation in reproductive mode and transitional forms of pregnancy

Abstract

How innovations such as vision, flight and pregnancy evolve is a central question in evolutionary biology. Examination of transitional (intermediate) forms of these traits can help address this question, but these intermediate phenotypes are very rare in extant species. Here we explore the biology and evolution of transitional forms of pregnancy that are midway between the ancestral state of oviparity (egg‐laying) and the derived state, viviparity (live birth). Transitional forms of pregnancy occur in only three vertebrates, all of which are lizard species that also display intraspecific variation in reproductive phenotype. In these lizards (Lerista bougainvillii, Saiphos equalis, and Zootoca vivipara), geographic variation of three reproductive forms occurs within a single species: oviparity, viviparity, and a transitional form of pregnancy. This phenomenon offers the valuable prospect of watching ‘evolution in action’. In these species, it is possible to conduct comparative research using different reproductive forms that are not confounded by speciation, and are of relatively recent origin. We identify major proximate and ultimate questions that can be addressed in these species, and the genetic and genomic tools that can help us understand how transitional forms of pregnancy are produced, despite predicted fitness costs. We argue that these taxa represent an excellent prospect for understanding the major evolutionary shift between egg‐laying and live birth, which is a fundamental innovation in the history of animals.

Natural variation in theCaenorhabditis elegansegg-laying circuit modulates an intergenerational fitness trade-off

“…In extreme cases of strong constitutive egg retention, C. elegans strains exhibit partial viviparity, associated with significantly reduced maternal reproduction and survival. Overall, observed genetically variable duration of intra-uterine development in C. elegans thus seems to align well with past reports showing that transitions towards viviparity incur maternal fitness costs as observed for diverse invertebrate and vertebrate taxa with both inter- and intraspecific differences in parity modes (Avise, 2013; Blackburn, 2015; Horváth and Kalinka, 2018; Kalinka, 2015; Ostrovsky et al, 2015; Whittington et al, 2022). To what extent this apparent intergenerational fitness trade-off in C. elegans could involve shaped by parent-offspring conflict (Trivers, 1974) is uncertain.…”

Selection on many loci drove the origin and spread of a key innovation

“…A recent transition from egg-laying to live-birth provides a rare opportunity to study the genetic architecture of a well-studied innovation whose origins and genetic basis are not well documented ( 4 ). We focus on a clade of intertidal gastropods (Genus Littorina ), where the ancestral state is to lay a large egg-mass but one species gives birth to live young (Fig.…”

“…Due to the complexity of the trait and number of associated loci, it is unlikely that live-birth arose in a single mutational step, as suggested by models of saltational evolution ( 17 ). Rather, live birth probably evolved gradually as a by-product of selection on related reproductive traits, such as embryo retention time ( 4 ). Live-bearing snails then eventually spread north, bringing them into contact with egg-layers.…”

The diverse terminology of reptile eggshell microstructure and its effect on phylogenetic comparative analyses

“…The reproductive strategies of these groups have been studied in the context of their respective radiations, with some traits identified as major factors of their evolutionary success – e.g. egg shape and size in birds (Birchard & Deeming, 2015; Birkhead et al, 2019; Deeming, 2007, 2018a; Deeming & Ruta, 2014; Duursma et al, 2018; Dyke & Kaiser, 2010; Mytiai et al, 2017, 2021; Nagy et al, 2019; Stoddard et al, 2017), or the high flexibility of reproductive traits in squamates, which facilitated their many independent acquisitions of viviparity (Andrews & Mathies, 2000; Blackburn, 1993, 2000a, 2000b, 2006; Blackburn & Stewart, 2021; Griffith et al, 2015; Pyron & Burbrink, 2014; Shine, 1995, 2005; Sites et al, 2011; Stewart, 2013, 2015; Stewart & Thompson, 2000; Whittington et al, 2022).…”