Sexual antagonism and sex determination in three syngnathid species alongside a male pregnancy gradient

Abstract

Teleost fish show an enormous diversity of sex determination systems, varying from environmental sex determination to full sex chromosomes. Traditionally sex chromosomes are considered within a framework of sexually antagonistic relationships and are viewed not only as sex determination systems but also as a means to resolve sexual conflict by confining conflicting genes to one sex. However, the relationship between emergence sexually-antagonistic loci, resolution of sexual conflict and sex determination is not fully understood. In this study we take a look at genomic and transcriptomic signatures of sexual antagonism, and relate them to putative sex determination systems in three species from the family Syngnathidae: Nerophis ophidion, Syngnathus typhle and Hippocampus erectus. The family is famous for their extreme form of parental care - male pregnancy. Male pregnancy forms a parental investment gradient among species of the family. We selected species alongside this gradient to investigate the effects male pregnancy has on sexual conflict in syngnathids. We found that both S.typhle and N.ophidion seem to have environmental sex determination and that sexual conflict is primarily resolved via differential gene and allele expression. On the other hand H.erectus possess an XY sex chromosome system. Strikingly, the identified homomorphic Y chromosome is not homologous to the Y chromosome of H.erectus identified in an independent study. We hypothesize that both sex-linked chromosomes evolved due to captive breeding and represent transition states between sex determination systems. Furthermore, we propose that the master sex determination gene is located outside of these sex-linked chromosomes.

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

“…We found that the gonads especially, but livers as well, displayed sex-biased patterns of expression, and the genes that were sex-biased in one organ were generally not sex-biased in the others. In the gills, which do not serve a reproductive function, we observed only a small number of differentially expressed genes, but those that were differentially expressed generally were related to immunity, similar to other pipefishes (Dubin et al, 2023;Pappert et al, 2023). Genes that had the largest bias in expression while still being expressed in both sexes also tended to be tissue specific in their expression patterns, suggesting that sex-biased expression might more readily evolve in genes with fewer pleiotropic constraints.…”

“…Several sex-specific genes reinforce this pattern of sex differences in immune function in the gill, such as vascular cell adhesion protein 1 and galactose-specific lectin nattectin, which are male-specific in both gonads and gills and have been shown in zebrafish and multiple finfish to be related to immune responses (Elumalai et al, 2019;Hsieh et al, 2018). Differences in immune function between males and females have previously been demonstrated in pipefish (Dubin et al, 2023;Pappert et al, 2023;Roth et al, 2011), and the male-specific patterns of expression we observed could support the hypothesis the pregnant male pipefish experience different selection pressures with regard to immunity compared to female and non-pregnant pipefish (J. Parker et al, 2023;Roth et al, 2020).…”

“…However, in S. floridae, this gene showed a male-specific expression pattern in the gills, which do not have a reproductive function. The gene cathepsin K had sexspecific alleles in S. typhle (Dubin et al, 2023) was female-specific in the gonads in our dataset.…”

“…Another factor that could impact these patterns is the lack of a known sex determination system in these pipefish. Within syngnathids, variation in sex determination systems exist, with evidence for a single male-specific sex-determining locus in sea dragons and some pipefish (Qu et al, 2021), a genomic region consistent with XY patterns of inheritance in a seahorse (Long et al, 2022), and no obvious genetic region associating with sex in Syngnathus scovelli (Ramesh et al, 2023;Small et al, 2016) or Syngnathus typhle (Dubin et al, 2023). Due to the close phylogenetic relationship between S. floridae and other Syngnathus species (Hamilton et al, 2017), we view it is unlikely that a sex-specific region of the genome exists.…”

“…Any genes experiencing sexually antagonistic selection arising from post-copulatory sexual conflict are most likely autosomal, and found in genomes of both sexes, given that the other Syngnathus species do exhibit evidence of diverged sex chromosomes (Dubin et al, 2023;Long et al, 2022;Ramesh et al, 2023;Small et al, 2016). As such, any sexual dimorphism, in size or expression, will arise from genetic architecture present in both sexes.…”