Biology subjects

Powell, D. L.

Publications and source records attributed to Powell, D. L..

16 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

Insertion of an invading retrovirus regulates a novel color trait in swordtail fish

For over a century, evolutionary biologists have been motivated to understand the mechanisms through which organisms adapt to their environments. Coloration and pigmentation are remarkably variable within and between species and can serve as an important window into the mechanisms of adaptation. Here, we map the genetic basis of a newly described iridescence trait in swordtail fish to a single locus. Individuals with this trait appear to sparkle as they move through the water. We find that the trait is driven by the recent endogenization of a retrovirus that inserted near the gene alkal2a. This insertion is associated with changes in the chromatin landscape, upregulation of alkal2a, and accumulation of iridescent cells that adhere to the scales. Rather than causing diseases, our results demonstrate that invading endogenous retroviruses can also regulate novel trait variation in the host. Moreover, we find that this coloration trait may act as an important signal in interactions between fish and their predators in the natural environment.

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

Recurrent evolution of small body size and loss of the sword ornament in Northern Swordtail fish

Across the tree of life, species have repeatedly evolved similar phenotypes. While well-studied for ecological traits, there is also evidence for convergent evolution of sexually selected traits. Swordtail fish (Xiphophorus) are a classic model system for studying sexual selection, and female Xiphophorus exhibit strong mate preferences for large male body size and a range of sexually dimorphic ornaments. However, sexually selected traits have been lost multiple times in the genus. Phylogenetic relationships between species in this group have historically been controversial, likely as a result of prevalent gene flow, resulting in uncertainty over the number of losses of ornamentation and large body size. Here, we use whole-genome sequencing approaches to re-examine phylogenetic relationships within a Xiphophorus clade that varies in the presence and absence of sexually selected traits. Using wild-caught individuals, we determine the phylogenetic placement of a small, unornamented species, X. continens, confirming an additional loss of ornamentation and large body size in the clade. With these revised phylogenetic relationships, we analyze evidence for coevolution between body size and other sexually selected traits using a phylogenetically independent contrasts approach. These results provide insights into the evolutionary pressures driving the recurrent loss of suites of sexually selected traits.

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↗

bioRxiv2022

A widely-used pollutant causes reversal of conspecific mate preference in a freshwater fish

Chemical communication is an important mechanism of mate choice across the animal tree of life. However, anthropogenic perturbation of the signaling environment can disrupt chemical communication and result in a breakdown of behavioral reproductive isolation. Here we find that calcium hydroxide (Ca(OH)2), a common and deliberately introduced anthropogenic pollutant, profoundly disrupts chemical communication in the swordtail fish Xiphophorus birchmanni. Moreover, it acts in a way that should promote hybridization, causing female X. birchmanni to prefer the chemical cues of the parapatric sister species X. malinche. We find that this flip in the direction of preference is attributable both to a reduced preference for conspecific signals and to a coupled strengthening of preference for sister-species signals.

animal behavior and cognition↗

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↗

bioRxiv2021

Predictability and parallelism in the contemporary evolution of hybrid genomes

Hybridization between species is widespread across the tree of life. As a result, many species, including our own, harbor regions of their genome derived from hybridization. Despite the recognition that this process is widespread, we understand little about how the genome stabilizes following hybridization, and whether the mechanisms driving this stabilization tend to be shared across species. Here, we dissect the drivers of variation in local ancestry across the genome in replicated hybridization events between two species pairs of swordtail fish: Xiphophorus birchmanni x X. cortezi and X. birchmanni x X. malinche. We find unexpectedly high levels of repeatability in local ancestry across the two types of hybrid populations. This repeatability is attributable in part to the fact that the recombination landscape and locations of functionally important elements play a major role in driving variation in local ancestry in both types of hybrid populations. Beyond these broad scale patterns, we identify dozens of regions of the genome where minor parent ancestry is unusually low or high across species pairs. Analysis of these regions points to shared sites under selection across species pairs, and in some cases, shared mechanisms of selection. We show that one such region is a previously unknown hybrid incompatibility that is shared across X. birchmanni x X. cortezi and X. birchmanni x X. malinche hybrid populations.

evolutionary biology↗

bioRxiv2020

Two new hybrid zones expand the swordtail hybridization model system

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 X. birchmanni from collection sites on two rivers. We develop sensitive and accurate local ancestry calling for this system based on low coverage whole genome sequencing. Strikingly, we find that hybrid populations on both rivers consist of two genetically distinct subpopulations: a cluster of nearly pure X. birchmanni individuals and one of phenotypically intermediate hybrids that derive ~85-90% of their genome from X. cortezi. Simulations and empirical data suggest that at both sites initial hybridization occurred ~150 generations ago, with little evidence for contemporary gene flow between subpopulations, likely due to strong assortative mating. The patterns of population structure uncovered here mirror those seen in hybridization between X. birchmanni and its sister species, X. malinche. Future comparisons will provide a window into the repeatability of the outcomes of hybridization not only across independent hybridization events between the same species but also across distinct species pairs.

evolutionary biology↗

bioRxiv2020

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

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.

evolutionary biology↗

bioRxiv2019

Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish

The establishment of reproductive barriers between populations is the key process that fuels the evolution of new species. A genetic framework for this process was proposed over 80 years ago, which posits "incompatible" interactions between genes that result in reduced survival or reproduction in hybrids. Despite this foundational work, progress has been slow in identifying individual genes that underlie hybrid incompatibilities, with only a handful known to date. Here, we use a combination of approaches to precisely map the genes that drive the development of a melanoma incompatibility in swordtail fish hybrids. We find that one of the genes involved in this incompatibility also causes melanoma in hybrids between distantly related species. Moreover, we show that this melanoma reduces survival in the wild, likely due to progressive degradation of the fin. Together, this work represents only the second case where the genes underlying a vertebrate hybrid incompatibility have been identified and provides the first glimpse into the action of these genes in natural hybrid populations. One sentence summaryUsing a combination of mapping approaches, we identify interacting genes that lead to melanoma in hybrids and characterize their effects in natural hybrid populations.

evolutionary biology↗

bioRxiv2019

Versatile simulations of admixture and accurate local ancestry inference with mixnmatch and ancestryinfer

It is now clear that hybridization between species is much more common than previously recognized. As a result, we now know that the genomes of many modern species, including our own, are a patchwork of regions derived from past hybridization events. Increasingly researchers are interested in disentangling which regions of the genome originated from each parental species using local ancestry inference methods. Due to the diverse effects of admixture, this interest is shared across disparate fields, from human genetics to research in ecology and evolutionary biology. However, local ancestry inference methods are sensitive to a range of biological and technical parameters which can impact accuracy. Here we present paired simulation and ancestry inference pipelines, mixnmatch and ancestryinfer, to help researchers plan and execute local ancestry inference studies. mixnmatch can simulate arbitrarily complex demographic histories in the parental and hybrid populations, selection on hybrids, and technical variables such as coverage and contamination. ancestryinfer takes as input sequencing reads from simulated or real individuals, and implements an efficient local ancestry inference pipeline. We perform a series of simulations with mixnmatch to pinpoint factors that influence accuracy in local ancestry inference and highlight useful features of the two pipelines. Together, mixnmatch and ancestryinfer are powerful tools for predicting the performance of local ancestry inference methods on real data.

genomics↗