Parallel Genomic Changes Drive Repeated Evolution of Placentas in Live-Bearing Fish

Abstract

The evolutionary origin of complex organs challenges empirical study because most organs evolved hundreds of millions of years ago. The placenta of live-bearing fish in the family Poeciliidae represents a unique opportunity to study the evolutionary origin of complex organs, because in this family a placenta evolved at least nine times independently. It is currently unknown whether this repeated evolution is accompanied by similar, repeated, genomic changes in placental species. Here we compare whole genomes of 26 poeciliid species representing six out of nine independent origins of placentation. Evolutionary rate analysis revealed that the evolution of the placenta coincides with convergent shifts in the evolutionary rate of 78 protein-coding genes, mainly observed in transporter- and vesicle-located genes. Furthermore, differences in sequence conservation showed that placental evolution coincided with similar changes in 76 non-coding regulatory elements, occurring primarily around genes that regulate development. The unexpected high occurrence of GATA simple repeats in the regulatory elements suggests an important function for GATA repeats in developmental gene regulation. The distinction in molecular evolution observed, with protein-coding parallel changes more often found in metabolic and structural pathways, compared to regulatory change more frequently found in developmental pathways, offers a compelling model for complex trait evolution in general: changing the regulation of otherwise highly conserved developmental genes may allow for the evolution of complex traits.

Genomic signatures associated with transitions to viviparity in Cyprinodontiformes

“…Independent acquisitions of placentotrophy in Poecilidae showed a preponderance of proteincoding genes undergoing shifts in sequence divergence in placental species compared to nonplacental species (van Kruistum, et al 2021). In our study, we did not find a higher incidence of convergence at any level examinedin fact we found a higher incidence of molecular convergence in our null models.…”

“…In particular, shifts in the expression of genes involved in hormonal regulation, tissue remodelling and nutrient exchange, as well as convergent loss of genes involved in adaptive immune response were found to coincide with the evolution of viviparity in these taxa. However, despite increasing availability of genomic data covering independent transitions to viviparity, there have been few explicit tests of genome-wide molecular convergence linked to viviparity and associated adaptations (Gao et al 2019;Roth et al 2020;van Kruistum et al 2021;Recknagel et al 2021). 100 Recently, Foster et al (2022) analysed the transcriptomes of the placenta of eight vertebrates (not including fish) and concluded that there was no significant overlap in gene involvement, so each placenta had evolved from unique changes in gene expression networks.…”

“…In poecilids, phylogenetic comparative methods have demonstrated that the evolution of matrotrophy and placentation is associated with sexual conflict and sexual selection (Pollux et al ., 2014; Furness et al ., 2019). Similarly, comparative genomic analyses within the order have specifically focused on understanding the genetic context of placental evolution, uncovering parallels with mammalian viviparity and between independent acquisitions of placentae in poecilids (Guernsey et al 2020; van Kruistum, et al 2021). The Goodeidae , a family of mostly viviparous ray-finned fish within the order Cyprindontiformes have received less attention.…”

BASE: A novel workflow to integrate nonubiquitous genes in comparative genomics analyses for selection

“…The inclusion of nonubiquitous genes should be applied with caution by the user: Too many missing species—both in the branches/clades of interest and/or in the whole tree—could impact evolutionary rates of inference. We suggest to either opt for (A) or to rely on conservative thresholds when opting for (B) (e.g., 90% of species present; van Kruistum et al., 2021 ).…”

Editorial: Ecology, Evolution, and Behavior of Viviparous Fishes

“…The second topic focuses on the extent to which convergent evolution in independent lineages is associated with parallel or alternative changes at the genomic level. Comparing the genomes of populations or species that independently evolved new phenotypic traits allows the identification of genomic differences associated with these phenotypes (Elmer and Meyer, 2011;Stern, 2013;van Kruistum et al, 2021). It is noteworthy to point out that such comparative approaches become statistically more powerful in identifying phenotype-related genes as the number of independent origins included in the study increases.…”