Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta

Abstract

The repeated evolution of the same traits in distantly related groups (convergent evolution) raises a key question in evolutionary biology: do the same genes underpin convergent phenotypes? Here, we explore one such trait, viviparity (live birth), which, qualitative studies suggest, may indeed have evolved via genetic convergence. There are >150 independent origins of live birth in vertebrates, providing a uniquely powerful system to test the mechanisms underpinning convergence in morphology, physiology, and/or gene recruitment during pregnancy. We compared transcriptomic data from eight vertebrates (lizards, mammals, sharks) that gestate embryos within the uterus. Since many previous studies detected qualitative similarities in gene use during independent origins of pregnancy, we expected to find significant overlap in gene use in viviparous taxa. However, we found no more overlap in uterine gene expression associated with viviparity than we would expect by chance alone. Each viviparous lineage exhibits the same core set of uterine physiological functions. Yet, contrary to prevailing assumptions about this trait, we find that none of the same genes are differentially expressed in all viviparous lineages, or even in all viviparous amniote lineages. Therefore, across distantly related vertebrates, different genes have been recruited to support the morphological and physiological changes required for successful pregnancy. We conclude that redundancies in gene function have enabled the repeated evolution of viviparity through recruitment of different genes from genomic "toolboxes", which are uniquely constrained by the ancestries of each lineage.

Keywords: complex traits; placentotrophy; viviparity.

Fig. 1.

UpSet plots visualizing the degree of overlap in enriched GO terms (a and b) and differentially expressed genes (c and d) across eight vertebrate species, taking into account parity mode and nutritional mode (placentotrophic vs. lecithotrophic embryonic nutrition). Vertical bars indicate overlaps that are greater than expected by chance alone, as determined using generalized Fisher’s exact tests. Horizontal bars represent the total number of enriched GO terms or differentially expressed orthogroups per species.

Fig. 2.

The phylogenetic relationships among the eight vertebrate species in our study, as well as their recruitment of AA-transporting SLC genes (AA SLCs) during gestation. All orthologous AA SLCs detected in the transcriptomes of our species are listed, and the recruitment of AA SLCs from this “toolbox” to different lineages is demonstrated using colored boxes. AA SLCs with orange boxes are upregulated by more than one lineage, and those with red boxes are specifically upregulated in only one lineage. Image credit for opossum silhouette: Sarah Werning (CC BY 3.0). V, viviparous; P, placentotrophic; L, lecithotrophic; O, oviparous.

Fig. 3.

Assessing the extent of convergence in gestation-related differential expression of orthologous genes across eight vertebrate species. (a) Phylogenetic tree for all species in our study, inferred using neighbor-joining analysis of a distance matrix of orthologous gene expression patterns. This “expression tree” is largely congruent with estimates of the species tree based on sequence data. (b) PCA of cross-sample normalized expression values for the eight species. The color of shapes is specific to each species, and the type of shape (circle vs. triangle) demonstrates the stage of gestation for each replicate sample (nongestating vs. gestating).