Genomic and transcriptomic investigations of the evolutionary transition from oviparity to viviparity

Abstract

Viviparous (live-bearing) vertebrates have evolved repeatedly within otherwise oviparous (egg-laying) clades. Over two-thirds of these changes in vertebrate reproductive parity mode happened in squamate reptiles, where the transition has happened between 98 and 129 times. The transition from oviparity to viviparity requires numerous physiological, morphological, and immunological changes to the female reproductive tract, including eggshell reduction, delayed oviposition, placental development for supply of water and nutrition to the embryo by the mother, enhanced gas exchange, and suppression of maternal immune rejection of the embryo. We performed genomic and transcriptomic analyses of a closely related oviparous–viviparous pair of lizards (Phrynocephalus przewalskii and Phrynocephalus vlangalii) to examine these transitions. Expression patterns of maternal oviduct through reproductive development of the egg and embryo differ markedly between the two species. We found changes in expression patterns of appropriate genes that account for each of the major aspects of the oviparity to viviparity transition. In addition, we compared the gene sequences in transcriptomes of four oviparous–viviparous pairs of lizards in different genera (Phrynocephalus, Eremias, Scincella, and Sphenomorphus) to look for possible gene convergence at the sequence level. We discovered low levels of convergence in both amino acid replacement and evolutionary rate shift. This suggests that most of the changes that produce the oviparity–viviparity transition are changes in gene expression, so occasional reversals to oviparity from viviparity may not be as difficult to achieve as has been previously suggested.

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

“…Genes upregulated in gravidity within both oviparous and viviparous S. equalis are enriched for GO terms and KEGG pathways related to uterine remodelling, including extracellular structure organization, proteolysis, and peptidase activity (Tables S4-S5). The genes related to uterine remodelling in both oviparous and viviparous S. equalis are similar to those seen in other viviparous skinks and mammals (Brandley, Young, Warren, Thompson, & Wagner, 2012;Gao et al, 2019;Salamonsen & Nie, 2002…”

“…Collectively, many of the putative genes supporting internal gestation of embryos in both long egg-retaining oviparous and viviparous S. equalis are similar to those found in other viviparous squamates and mammals (Brandley et al, 2012;Gao et al, 2019;Hendrawan, Whittington, Brandley, Belov, & Thompson, 2017;Salamonsen & Nie, 2002). A key strength of our within-species study is that any similarities or differences in gene expression between oviparous and viviparous S. equalis are more likely to be directly associated with parity mode than in a cross-species comparison.…”

“…Gene expression in the maternal uterus of both species showed temporal changes in gene expression across the reproductive cycle that reflect many of the morphological, immunological, and physiological differences between oviparous and viviparous F I G U R E 1 Saiphos equalis and its distribution within Australia. (a) photograph of S. equalis from an oviparous population in the Sydney region (credit: Nicholas Wu), (b) the distribution of S. equalis (Atlas of Living Australia, February 2020), with the oviparous population from this study marked with a diamond, and the viviparous population marked with a star [Colour figure can be viewed at wileyonlinelibrary.com] species (Gao et al, 2019). However, cross-species comparisons such as this one risk conflating parity mode-specific adaptation with species-specific adaptations that are unrelated to the evolution of viviparity (Garland & Adolph, 1994;Stewart et al, 2010).…”

Comparative landscape genetics reveals the evolution of viviparity reduces genetic connectivity in fire salamanders

“…The evolution of derived phenotypic traits enables individuals to exploit novel resources and colonise new areas, often entailing profound eco‐evolutionary implications to taxa (Losos, ). One remarkable life‐history adaptation is the transition from egg‐laying (oviparous) reproduction to live‐bearing (viviparous) reproduction, which occurred more than 150 times in vertebrates (mostly in reptiles) and involved major phenotypic, genetic, and ecological changes, especially in females (e.g., Blackburn, ; Gao et al, ; Halliwell, Uller, Holland, & While, ; Helmstetter et al, ; Pincheira‐Donoso, Tregenza, Witt, & Hodgson, ; Wake, ). Strong environmental pressures on offspring (e.g., stressful environmental conditions or predation) generally selected for longer periods of embryo retention (i.e., viviparity) to increase offspring survival rates, thus allowing viviparous taxa to thrive in harsher environments and disperse to areas previously inaccessible (e.g., Helmstetter et al, ; Ma, Buckley, Huey, & Du, ; Pincheira‐Donoso et al, ).…”

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 ., ).…”