The genetic architecture of the sexually selected sword ornament and its evolution in hybrid populations

Abstract

Biologists since Darwin have been fascinated by the evolution of sexually selected ornaments, particularly those that reduce viability. Uncovering the genetic architecture of these traits is key to understanding how they evolve and are maintained. Here, we investigate the genetic architecture of a sexually selected ornament, the “sword” fin extension that characterizes many species of swordtail fish (Xiphophorus). Using sworded and swordless sister species of Xiphophorus, we generated a mapping population and show that the sword ornament is polygenic – with ancestry across the genome explaining substantial variation in the trait. After accounting for the impacts of genome-wide ancestry, we identify one major effect QTL that explains ∼5% of the overall variation in the trait. Using a series of approaches, we narrow this large QTL interval to a handful of likely candidate genes, including the gene sp8. Notably, sp8 plays a regulatory role in fin regeneration and harbors several derived substitutions that are predicted to impact protein function in the species that has lost the sword ornament. Furthermore, we find evidence of selection on ancestry at sp8 in four natural hybrid populations, consistent with selection against the sword in these populations.

The developmental and genetic architecture of the sexually selected male ornament of swordtails

“…Our QTL analysis, consistent with earlier genetic findings [41], uncovered that several chromosomal regions contribute to the polygenic basis of the male structure. Consistently, the major locus on chromosome 13 fully overlaps a similar broad QTL that was obtained in an independent study for the character sword length in natural hybrids between a swordless (X. birchmanni) and a sworded (X. malinche) Northern swordtail species [48].We identified two candidate genes that appear to be involved in the development of the sword. Rather than being typical regulators of development and differentiation such as transcription factors or extracellular diffusible growth factors, experiments identified a channel protein, kcnh8, and a chaperone, fkpb9.…”

The genomic consequences of hybridization

“…This can result in an incompatibility generated by misregulation and transgressive expression of such genes in hybrids. ( A ) tspan8 (left) and pkma (right) are examples of genes for which swordtail hybrids exhibit low and high misexpression, respectively (MM: X. malinche ; BB: X. birchmanni ; MB: F 1 hybrids; data from Powell et al, 2021 ). ( B ) This simplified diagram illustrates how mismatches in co-evolved regulatory elements can cause misexpression.…”

Predictability and parallelism in the contemporary evolution of hybrid genomes

“…As expected from the cross design, average ancestry across ancestry informative sites in our dataset of 943 males and females indicated that on average 50% of the genome was derived from each parental species. Our previously published dataset for QTL mapping included 568 males [66].…”

“…We also recently generated a large mapping panel of F2 hybrids between X. birchmanni ´ X. malinche, which we used for QTL mapping of male sexually selected traits [66]. Here, we reanalyzed this mapping panel, doubling our sample size by including females, to identify strong segregation distorters.…”