Biology subjects

Gunn, T. R.

Publications and source records attributed to Gunn, T. R..

8 recordsLinked to original sources

bioRxiv2026

Two melanic pigment patterns are associated with a sex chromosome-linked oncogene in the mountain swordtail Xiphophorus nezahualcoyotl

Sex-linked traits are widespread, but their genetic architecture has been challenging to characterize, due in part to the repetitive and structurally complex nature of sex chromosomes. In swordtails and platyfish of the genus Xiphophorus, diverse melanic pigmentation patterns are thought to be controlled by a region on the sex chromosomes classically referred to as the "macromelanophore determining locus". Despite nearly a century of study, the identity of the causal gene remains controversial, partially due to previous inability to fully sequence the sex chromosomes. Here, we characterize and investigate two melanin-based pigmentation phenotypes in the species X. nezahualcoyotl: "spotted side" and "marmoratus". We generate a gapless near-telomere-to-telomere X. nezahualcoyotl assembly and perform GWAS to identify regions associated with pigmentation pattern variation and sex-determination. We find both patterns map near the sex-determining region and to a narrow interval near the oncogene xmrk. By generating additional long-read assemblies of sex chromosomes derived from individuals with distinct phenotypes, we find haplotypes containing xmrk can be both X- and Y-linked, and vary dramatically in gene content, structure, and accumulation of repetitive elements including a newly described composite satellite. This variability may impact the regions stability and affect recombination between haplotypes associated with each pattern. Our results shed light on a longstanding debate surrounding the genetic architecture of sex-linked phenotypes. More generally, we showcase how long-read sequencing can reveal phenotypic variation linked to complex and dynamic genomic regions, which may contribute to the evolution of diverse sex-linked traits.

evolutionary biology↗

bioRxiv2025

Increased rates of hybridization in swordtail fish are associated with water pollution

Understanding the nature of reproductive barriers separating species is a fundamental goal of evolutionary biology. Such barriers may be environmentally sensitive, and recent research has documented an increasing number of cases where anthropogenic environmental disturbance is associated with hybridization. However, few studies have been able to quantify and compare potential environmental mechanisms connecting anthropogenic disturbance to hybridization. Here, we combine genomic and environmental surveys to explore the loss of reproductive isolation between Xiphophorus malinche and X. birchmanni, fishes whose riverine habitat in montane Mexico is increasingly impacted by human-mediated disturbance. By inferring genome-wide ancestry in thousands of fish, we characterize the landscape of hybridization between these sister species in four drainages. Ancestry structure varies across streams from stable coexistence to clinal hybrid zones, hinting that hybridization dynamics in this system may be environmentally dependent. In one stream, sites upstream of an urbanized area host distinct sympatric ancestry clusters, while downstream sites collapse into a hybrid swarm. By sequencing mothers and embryos, we show that assortative mating is weakened downstream of this urbanized area. We hypothesize that the downstream hybrid swarm is driven by chemical disruption of olfaction that impacts mating preferences. Water chemistry measurements show significant changes across the urbanized area, including in parameters known to disrupt fish olfaction and mating. We identify alterations of the olfactory epithelium between sites upstream and downstream of the urbanized area consistent with differential effects of water quality. Taken together, our work illuminates potential mechanisms linking anthropogenic disturbance to the breakdown of reproductive isolation.

evolutionary biology↗

bioRxiv2024

Complex structural variation and behavioral interactions underpin a balanced sexual mimicry polymorphism

How phenotypic diversity originates and persists within populations are classic puzzles in evolutionary biology. While polymorphisms hypothesized to be under balancing selection segregate within many species, it remains rare for the genetic basis and the selective forces to both be known for the same trait, leading to an incomplete understanding of many classes of polymorphisms. Here, we uncover the genetic architecture of a balanced sexual mimicry polymorphism and identify behavioral mechanisms that may be involved in its maintenance in the swordtail fish Xiphophorus birchmanni. We find that [~]40% of X. birchmanni males develop a "false gravid spot", a melanic pigmentation pattern that mimics the "pregnancy spot" associated with sexual maturity in female live-bearing fish. Using genome-wide association mapping, we detect a single intergenic region associated with variation in the false gravid spot, which is upstream of kitlga, a gene involved in melanophore patterning. By performing long-read sequencing within and across populations, we identify complex structural rearrangements between alternate alleles at this locus. The false gravid spot haplotype drives increased allele-specific expression of kitlga, which provides a mechanistic explanation for the increased melanophore abundance that causes the spot. By studying social interactions in the laboratory and in nature, we find that males with the false gravid spot experience less aggression; however, they also receive increased attention from other males and are disdained by females. These behavioral interactions may play a role in maintaining this phenotypic polymorphism in natural populations. We speculate that structural variants affecting gene regulation may be an underappreciated driver of balanced polymorphisms across diverse species.

evolutionary biology↗

bioRxiv2024

Pervasive gene flow despite strong and varied reproductive barriers in swordtails

One of the mechanisms that can lead to the formation of new species occurs through the evolution of reproductive barriers. However, recent research has demonstrated that hybridization has been pervasive across the tree of life even in the presence of strong barriers. Swordtail fishes (genus Xiphophorus) are an emerging model system for studying the interface between these barriers and hybridization. We document overlapping mechanisms that act as barriers between closely related species, X. birchmanni and X. cortezi, by combining genomic sequencing from natural hybrid populations, artificial crosses, behavioral assays, sperm performance, and developmental studies. We show that strong assortative mating plays a key role in maintaining subpopulations with distinct ancestry in natural hybrid populations. Lab experiments demonstrate that artificial F1 crosses experience dysfunction: crosses with X. birchmanni females were largely inviable and crosses with X. cortezi females had a heavily skewed sex ratio. Using F2 hybrids we identify several genomic regions that strongly impact hybrid viability. Strikingly, two of these regions underlie genetic incompatibilities in hybrids between X. birchmanni and its sister species X. malinche. Our results demonstrate that ancient hybridization has played a role in the origin of this shared genetic incompatibility. Moreover, ancestry mismatch at these incompatible regions has remarkably similar consequences for phenotypes and hybrid survival in X. cortezi O X. birchmanni hybrids as in X. malinche O X. birchmanni hybrids. Our findings identify varied reproductive barriers that shape genetic exchange between naturally hybridizing species and highlight the complex evolutionary outcomes of hybridization. Significance StatementBiologists are fascinated by how the diverse species we see on Earth have arisen and been maintained. One driver of this process is the evolution of reproductive barriers between species. Despite the commonality of these barriers, many species still exchange genes through a process called hybridization. Here, we show that related species can have a striking array of reproductive barriers--from genetic interactions that harm hybrids to mate preferences that reduce hybridization in the first place. However, we also find that genetic exchange between these species is very common, and may itself play an important role in the evolution of reproductive barriers. Together, our work highlights the complex web of interactions that impact the origin and persistence of distinct species.

evolutionary biology↗

bioRxiv2023

Genome evolution is surprisingly predictable after initial hybridization

Over the past two decades, evolutionary biologists have come to appreciate that hybridization, or genetic exchange between distinct lineages, is remarkably common - not just in particular lineages but in taxonomic groups across the tree of life. As a result, the genomes of many modern species harbor regions inherited from related species. This observation has raised fundamental questions about the degree to which the genomic outcomes of hybridization are repeatable and the degree to which natural selection drives such repeatability. However, a lack of appropriate systems to answer these questions has limited empirical progress in this area. Here, we leverage independently formed hybrid populations between the swordtail fish Xiphophorus birchmanni and X. cortezi to address this fundamental question. We find that local ancestry in one hybrid population is remarkably predictive of local ancestry in another, demographically independent hybrid population. Applying newly developed methods, we can attribute much of this repeatability to strong selection in the earliest generations after initial hybridization. We complement these analyses with time-series data that demonstrates that ancestry at regions under selection has remained stable over the past [~]40 generations of evolution. Finally, we compare our results to the well-studied X. birchmannixX. malinche hybrid populations and conclude that deeper evolutionary divergence has resulted in stronger selection and higher repeatability in patterns of local ancestry in hybrids between X. birchmanni and X. cortezi.

evolutionary biology↗

bioRxiv2023

Recent evolution of large offspring size and post-fertilization nutrient provisioning in swordtails

Organisms have evolved diverse reproductive strategies that impact the probability that their offspring survive to adulthood. Here, we describe divergence in reproductive strategy between two closely related species of swordtail fish (Xiphophorus). Swordtail fish and their relatives have evolved viviparity: they have internal fertilization and give birth to fully developed fry. We find that one species, X. malinche, which lives in high-elevation environments, has evolved larger offspring than its closest relative X. birchmanni and dwarfs the offspring size of other species in the genus. The larger fry of X. malinche are more resilient to starvation than their X. birchmanni relatives, hinting that the evolution of large offspring size may be an adaptation to the particularly challenging environments in which X. malinche are born. We find evidence that X. malinche achieves larger offspring size in part by continuing to provision their offspring over the course of embryonic development after fertilization, the first time this process has been documented in the Xiphophorus genus. Moreover, we observe differential regulation in the ovary of genes associated with maternal nutrient provisioning in other species that use this reproductive strategy. Intriguingly, these reproductive differences may drive an asymmetric hybrid incompatibility, since X. birchmanni mothers pregnant with F1 embryos give birth to premature and stillborn fry at an exceptionally high rate.

evolutionary biology↗

bioRxiv2022

Complex hybridization between deeply diverged fish species in a disturbed ecosystem

Over the past two decades researchers have documented the extent of natural hybridization between closely related species using genomic tools. Many species across the tree of life show evidence of past hybridization with their evolutionary relatives. In some cases, this hybridization is complex - involving gene flow between more than two species. While hybridization is common over evolutionary timescales, some researchers have proposed that it may be even more common in contemporary populations where anthropogenic disturbance has modified myriad aspects of the environments in which organisms live and reproduce. Here, we develop a flexible tool for local ancestry inference in hybrids derived from three source populations and describe a complex, recent hybridization event between distantly related swordtail fish lineages (Xiphophorus) and its potential links to anthropogenic disturbance. Impact SummaryAs sequencing tools have advanced, we have found that barriers between animal species are more porous than once thought. Researchers have found evidence for hybridization between species throughout many branches of the tree of life. In some cases, these hybridization events can involve more than two species. Here, we develop a flexible and user-friendly tool that can be used to identify three-way hybrids and report the discovery of hybrids with ancestry from three swordtail (Xiphophorus) species from an anthropogenically impacted site on the Rio Calnali in Hidalgo, Mexico. Researchers have studied hybrids between two Xiphophorus species along this river for decades, but this is the first documented case of hybridization involving three species. We explore hypotheses for what drove this hybridization event, including anthropogenic pollutants and reduced water quality.

evolutionary biology↗

bioRxiv2021

A Lethal Genetic Incompatibility between Naturally Hybridizing Species in Mitochondrial Complex I

The evolution of reproductive barriers is the first step in the formation of new species and can help us understand the diversification of life on Earth. These reproductive barriers often take the form of "hybrid incompatibilities," where alleles derived from two different species no longer interact properly in hybrids. Theory predicts that hybrid incompatibilities may be more likely to arise at rapidly evolving genes and that incompatibilities involving multiple genes should be common, but there has been sparse empirical data to evaluate these predictions. Here, we describe a mitonuclear incompatibility involving three genes in physical contact within respiratory Complex I in naturally hybridizing swordtail fish species. Individuals homozygous for specific mismatched protein combinations fail to complete embryonic development or die as juveniles, while those heterozygous for the incompatibility have reduced function of Complex I and unbalanced representation of parental alleles in the mitochondrial proteome. We find that the impacts of different genetic interactions on survival are non-additive, highlighting subtle complexity in the genetic architecture of hybrid incompatibilities. We document the evolutionary history of the genes involved, showing for the first time that an incompatibility has been transferred between species via hybridization. This work thus provides the first glimpse into the genetic architecture, physiological impacts, and evolutionary origin of a complex incompatibility impacting naturally hybridizing species.

evolutionary biology↗