The Developmental and Genetic Architecture of the Sexually Selected Male Ornament of Swordtails

Schartl, Manfred; Kneitz, Susanne; Ormanns, Jenny; Schmidt, Cornelia; Anderson, Jennifer; Amores, Angel; Catchen, Julian M.; Wilson, Catherine; Geiger, Dietmar; Du, Kang; García-Olazábal, Mateo; Sudaram, Sudha; Winkler, Christoph; Hedrich, Rainer; Warren, Wesley C.; Walter, Ronald B.; Meyer, Axel; Postlethwait, John H.

doi:10.1016/j.cub.2020.11.028

Cited by 27 publications

(32 citation statements)

References 78 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…birchmanni (Fig 3) and an overall rapid rate of protein evolution between X. birchmanni and X. malinche (dN/dS = 0.78; upper 3% genome-wide) [32]. Although sp8 harbors a large number of substitutions derived in X. birchmanni (Fig 3), we did not find strong evidence for a different substitution rate along the X. birchmanni branch based on PAML analysis (c 2 =3, p=0.08).…”

Section: Fig 2 Ancestry At Chromosome 13 and Throughout The Genome Contributes To Sword Lengthmentioning

confidence: 69%

See 1 more Smart Citation

The Genetic Architecture of Variation in the Sexually Selected Sword Ornament and Its Evolution in Hybrid Populations

et al. 2021

View full text Add to dashboard Cite

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..

show abstract

Section: Fig 2 Ancestry At Chromosome 13 and Throughout The Genome Contributes To Sword Lengthmentioning

confidence: 69%

“…Bootstrapping and joint analysis with another study allowed us to narrow this large interval to 1.2 Mb ( [32]; Supporting Information 2).…”

Section: Mapping the Genetic Basis Of The Sword Phenotypementioning

confidence: 99%

The Genetic Architecture of Variation in the Sexually Selected Sword Ornament and Its Evolution in Hybrid Populations

et al. 2021

View full text Add to dashboard Cite

show abstract

“…This QTL also contributes to variation in sword length in other species in the genus (Schartl et al. 2021). We examined local ancestry in hybrids from the Santa Cruz and Huextetitla populations within this region, focusing on the most promising candidate gene identified—the regulator of fin and limb development sp8 .…”

Section: Resultsmentioning

confidence: 99%

Two new hybrid populations expand the swordtail hybridization model system

et al. 2021

View full text Add to dashboard Cite

Natural hybridization events provide unique windows into the barriers that keep species apart as well as the consequences of their breakdown. Here, we characterize hybrid populations formed between the northern swordtail fish Xiphophorus cortezi and Xiphophorus birchmanni from collection sites on two rivers. We use simulations and new genetic reference panels to develop sensitive and accurate local ancestry calling in this novel system. Strikingly, we find that hybrid populations on both rivers consist of two genetically distinct subpopulations: a cluster of pure X. birchmanni individuals and one of phenotypically intermediate hybrids that derive ∼85–90% of their genome from X. cortezi. Simulations suggest that initial hybridization occurred ∼150 generations ago at both sites, with little evidence for contemporary gene flow between subpopulations. This population structure is consistent with strong assortative mating between individuals of similar ancestry. The patterns of population structure uncovered here mirror those seen in hybridization between X. birchmanni and its sister species, Xiphophorus malinche, indicating an important role for assortative mating in the evolution of hybrid populations. Future comparisons will provide a window into the shared mechanisms driving the outcomes of hybridization not only among independent hybridization events between the same species but also across distinct species pairs.

show abstract

“…The inversion results in ectopic overexpression of the voltage-gated potassium channel kcnh2a in the fin ( Fig 4 ) which we show is sufficient to drive coordinated overgrowth of the fin. This finding adds to a growing body of evidence that potassium channels and bioelectric signaling are instrumental in regulating fin size [16,24,33]. It is unknown whether there is a specific role for Kcnh2a protein in fin growth, or if kcnh2a is just one of many potassium channels where overexpression is sufficient to drive fin overgrowth [18,24].…”

Section: Discussionmentioning

confidence: 85%

Novel regulators of growth identified in the evolution of fin proportion in flying fish

Blum

Lanni

et al. 2021

Preprint

View full text Add to dashboard Cite

Identifying the genetic foundations of trait variation and evolution is challenging as it is often difficult to parse meaningful signals from confounding signatures such as drift and epistasis. However, identification of the genetic loci underlying morphological and physiological traits can be honed through the use of comparative and complementary genetic approaches, whereby shared sets of genes that are repeatedly implicated across large evolutionary time periods as under selection can illuminate important pathways and epistatic relationships that function as novel regulators of trait development. Here we intersect comparative genomic analyses with unbiased mutagenesis screens in distantly related species to define the control of proportional growth, as changes in the size and relative proportions of tissues underlie a large degree of the variant forms seen in nature. Through a phylogenomic analysis of genome-wide variation in 35 species of flying fishes and relatives, we identify genetic signatures in both coding and regulatory regions underlying the convergent evolution of increased paired fin size and aerial gliding behaviors, key innovations for flying fishes and flying halfbeaks. To refine our analysis, we intersected convergent phylogenomic signatures with mutants identified in distantly related zebrafish with altered fin size. Through these paired approaches, we identify a surprising role for an L-type amino acid transporter, lat4a, and the potassium channel, kcnh2a, in the regulation of fin proportion. We show that specific epistatic interaction between these genetic loci in zebrafish closely phenocopies the observed fin proportions of flying fishes. The congruence of experimental and phylogenomic findings point to a conserved, non-canonical signaling interaction that integrates bioelectric cues and amino acid transport in the establishment of relative size in development and evolution.

show abstract

The Developmental and Genetic Architecture of the Sexually Selected Male Ornament of Swordtails

Cited by 27 publications

References 78 publications

The Genetic Architecture of Variation in the Sexually Selected Sword Ornament and Its Evolution in Hybrid Populations

The Genetic Architecture of Variation in the Sexually Selected Sword Ornament and Its Evolution in Hybrid Populations

Two new hybrid populations expand the swordtail hybridization model system

Novel regulators of growth identified in the evolution of fin proportion in flying fish

Contact Info

Product

Resources

About