The evolution of the testis transcriptome in pregnant male pipefishes and seahorses

Abstract

In many animals, sperm competition and sexual conflict are thought to drive the rapid evolution of male‐specific genes, especially those expressed in the testes. A potential exception occurs in the male pregnant pipefishes, where females transfer eggs to the males, eliminating testes from participating in these processes. Here, we show that testis‐related genes differ dramatically in their rates of molecular evolution and expression patterns in pipefishes and seahorses (Syngnathidae) compared to other fish. Genes involved in testis or sperm function within syngnathids experience weaker selection in comparison to their orthologs in spawning and livebearing fishes. An assessment of gene turnover and expression in the testis transcriptome suggests that syngnathids have lost (or significantly reduced expression of) important classes of genes from their testis transcriptomes compared to other fish. Our results indicate that more than 50 million years of male pregnancy have removed syngnathid testes from the molecular arms race that drives the rapid evolution of male reproductive genes in other taxa.

Navigating sex and sex roles: deciphering sex-biased gene expression in a species with sex-role reversal ( Syngnathus typhle )

“…However, there were not many other pathways specifically related to generating sperm and associated fluids/proteins. These results are consistent with research in S. scovelli , where a reduced expression of genes associated with sperm function was found, suggesting that pipefish may have evolved to produce a smaller number of sperm [ 77 ]. The study also suggests that due to the selection for male pregnancy, this could potentially lead to a decrease in sperm count and shift energetic demands towards developing the brood pouch itself.…”

“…The gonads of male pipefish also revealed pathways associated with sperm quality and ejaculate volume such as metal ion or calcium transport ( figure 3 b ), including metallopeptidase and metalloproteinase genes (electronic supplementary material, table S3, gonads) [ 77 ]. However, there were not many other pathways specifically related to generating sperm and associated fluids/proteins.…”

Sexual selection on non-ornamental traits is underpinned by evidence of genetic constraints on sex-biased expression in dusky pipefish

“…Possibly genes with female-biased expression are somewhat more constrained in their expression, such that they must still be expressed at reasonable levels in males and require higher degrees of tissue specificity to reach high levels of sex-bias. If male-biased genes are less constrained, it could be related to relaxed selection on male syngnathid reproductive genes (Johnson et al, 2022).…”

“…In contrast, some genes have more tissue-specific patterns of expression, such as reproductive proteins (Segami et al, 2022), which might experience fewer evolutionary constraints. These tissue-specific genes often have sex-specific functions (Torgerson et al, 2005) and rapid rates of evolution (Harrison et al, 2015;Swanson & Vacquier, 2002) due to either positive selection, potentially to resolve conflict (Swanson & Vacquier, 2002), or due to the relaxation of selection (Dapper & Wade, 2020;Johnson et al, 2022). Importantly, if constraints prevent the decoupling of genetic architecture, even strong sexually antagonistic selection will be unable to drive the evolution of sexual dimorphism.…”