Biology subjects

Moran, R. L.

Publications and source records attributed to Moran, R. L..

15 recordsLinked to original sources

bioRxiv2026

Cave evolution on repeat: reuse of the same genomic regions across lineages but not across traits in Astyanax mexicanus

Similar traits repeatedly evolve across independent populations in response to similar environmental conditions. For many repeatedly evolved traits it is unknown if populations evolve similar traits through the same or different genetic mechanisms. To address this question, we leveraged the Mexican tetra fish, Astyanax mexicanus, which has evolved repeatedly through altering many traits including reduced sleep duration, eye degeneration, and metabolic shifts to accommodate limited nutrient availability. We defined whether shared or independent genetic architecture govern the repeated evolution of sleep loss, increased food consumption, early onset adipose deposition, and eye loss in different evolutionary origins of the cavefish phenotype by using Quantitative Trait Locus (QTL) mapping across three cave x surface F2 mapping populations. We found that, among the traits evaluated, eye loss exhibits the most genetic repeatability, with [~]43% of QTL shared across lineages. Sleep loss and metabolic traits (i.e., feeding, adiposity) were genetically less repeatable, with only [~]25-33% of QTL shared across lineages. Next, we explored whether QTL for metabolism, eye loss, and sleep traits in cavefish co-localize in the cavefish genome and could be inherited together to facilitate potential cavefish adaptation. Although these traits have repeatedly co-evolved in cave populations, we did not find evidence for extensive genetic linkage among them. Overall, we found that genetic repeatability is a common feature in the repeated evolution of cave traits, the extent of genetic repeatability varies across cave traits, and that there is little evidence for widespread co-localization of sleep, eye loss, and metabolic traits within the genome. SummaryIndependent populations that evolve similar traits in response to similar environmental conditions provide us with natural replicates for studying what constrains evolutionary change. Iconic examples of repeated trait evolution often involve repeated mutations in the same genes, suggesting there are limits on the type of genes and mutations that can contribute to phenotypic evolution. Here we conduct a multi-trait, multi-population QTL analysis for similar eye loss, sleep loss and metabolic shifts across two lineages of Astyanax mexicanus. Genetic repeatability is present for most traits, but its extent is highly trait dependent and occurs at the level of genomic regions rather than specific genes, highlighting the mosaic of constraint and flexibility involved in genetic repeatability.

evolutionary biology↗

bioRxiv2025

Environmental stress amplifies competitive asymmetry and drives divergent hybrid zone outcomes

Community persistence depends on the balance between abiotic constraints and biotic interactions. Environmental stress can either sort species by physiological limits or amplify competitive asymmetries, producing coexistence, exclusion, or collapse. We tested these alternatives in two replicate hybrid swarms between orangethroat and orangebelly darters (Etheostoma pulchellum and E. radiosum spp. complex) with contrasting outcomes: long-term coexistence in the Blue River versus collapse in the Washita River. We combined critical-thermal-maximum (CTmax) assays with standardized feeding experiments to evaluate physiological tolerance, competitive exclusion, and stress-amplified competition. CTmax varied with river, sex, and body size but not consistently between species, indicating that local history and demography outweighed intrinsic physiological differences. In contrast, competition trials revealed strong, temperature-dependent asymmetries: E. pulchellum dominated in the cooler, stable Blue River, whereas E. radiosum spp. gained a foraging advantage under high temperatures in the warmer Washita River drainage. These results support the prediction that abiotic stress amplifies competitive asymmetries, flipping dominance and explaining divergent hybrid zone outcomes. More broadly, our study links hybrid zone dynamics to coexistence theory, showing that climate extremes can shift competitive balance and determine whether secondary contact results in persistence or loss.

evolutionary biology↗

bioRxiv2025

The effect of environmental enrichment on whole-brain gene expression in an imperiled fish

When hatchery-reared fish are used to augment wild populations, phenotypic mismatch caused by differences between hatchery and wild environments can limit efforts to conserve fish species at risk of extinction. Some phenotypes adapted to or induced by hatchery environments are thought to be maladapted for life in the wild. Thus, enriching the hatchery environment (abiotically and biotically) to make it more similar to the wild may induce phenotypes, including gene expression profiles, that are better suited to the environments fish will experience after release. Here, we took a molecular approach (TagSeq) to elucidate how abiotic and biotic (predator training) enrichment impacts the whole-brain gene expression of a species of conservation concern, the Arkansas darter (Etheostoma cragini), comparing the effects in two hatchery populations to a wild reference population. While we found no effect of biotic enrichment, we found that numerous genes were differentially expressed between populations and abiotic enrichment treatments. Notably, we found that expression profiles of hatchery fish more closely resembled those of wild fish when reared with abiotic enrichment. Functional analysis revealed that many differentially expressed genes were related to feeding behavior, development, and reproduction. These results have implications for conservation, supporting the management of darters at the level of the population and the use of abiotic enrichment to reduce phenotypic mismatch between hatchery and wild fish.

molecular biology↗

bioRxiv2025

The genomic complexity of invasion: cryptic lineages, founder effects, and polygenic sex determination in armored catfish

Genetic biocontrol approaches offer promising tools for managing invasive species. However, their success depends on species identity, demographic history, and the genomic architecture of sex determination, which remain poorly resolved for many non-model taxa. We integrated high-quality genome assembly, whole-genome resequencing, and population genomics to evaluate biocontrol feasibility in invasive suckermouth armored catfish (Loricariidae) in Texas. Mitochondrial phylogenies and genome-wide SNPs revealed cryptic diversity, with distinct lineages from at least two genera (Hypostomus and Pterygoplichthys) exhibiting strong drainage-level genetic differentiation. Effective population size estimates were exceptionally low, consistent with founder effects and moderate inbreeding. Genome-wide association analyses detected no large-effect loci for sex in either genus, despite high statistical power in Hypostomus, suggesting that sex determination is polygenic and/or environmentally influenced. These results identify key biological constraints for sex-ratio-based biocontrol and underscore the importance of genomic assessments prior to management interventions. More broadly, our study highlights how integrating genomic resources, demographic inference, and evolutionary context can guide invasive species control strategies.

genetics↗

bioRxiv2025

Sex chromosome turnover and mitonuclear conflict drive reproductive isolation

Identifying the genetic basis of reproductive barriers is essential for understanding the origin and maintenance of biological diversity. While some hybrid incompatibilities evolve as incidental byproducts of divergence1-3, those involving sex chromosomes and mitochondrial-nuclear interactions may arise through predictable pathways shaped by genomic conflict4-8. Yet, the extent to which such interactions drive the evolution of reproductive barriers and speciation in natural populations remains unclear9-11. Here, we use whole-genome resequencing in North American fishes to show that two hybridizing species possess distinct, nonhomologous sex chromosomes. These chromosomes exhibit strong associations with sex, reduced introgression in natural hybrid zones, segregation distortion in backcrosses, and an enrichment of nuclear-encoded mitochondrial genes, indicative of sex-linked mitonuclear incompatibilities. We identify a third, distinct sex chromosome in another hybridizing species, indicating repeated sex chromosome turnover within the clade. Parental crosses and genomic analyses suggest that at least one of these transitions was driven by a recessive female-determining mutation, a rare empirical example of a theoretically predicted but seldom observed mechanism of sex chromosome evolution. Together, these results link genomic architecture to hybrid dysfunction and behavioral isolation, providing strong empirical support for long-standing predictions about the role of sex-linked and cytonuclear incompatibilities in speciation.

evolutionary biology↗

bioRxiv2024

Long-term hybridization in a karst window reveals the genetic basis of eye loss in cavefish

Eye loss is a hallmark trait of animals inhabiting perpetual darkness, yet the precise genetic variants underlying this evolutionary change remain largely unknown. The Mexican tetra (Astyanax mexicanus) provides a powerful model for dissecting the genetic basis of eye degeneration, as sighted surface fish and multiple independently evolved blind cave populations remain interfertile; yet despite decades of research and numerous QTL studies, the genetic basis of eye loss has remained unresolved at the level of specific variants. Here, we exploit a rare natural experiment in the Caballo Moro cave, where the collapse of a karst window created a partially illuminated pool inhabited by both fully eyed and completely eyeless cavefish of closely related genetic background. Whole-genome sequencing reveals a long-standing hybrid population between cave and surface lineages, enabling a dramatic refinement of the genetic architecture of eye degeneration to 203 candidate SNPs across 41 genes. Among these, we identified a nonsynonymous mutation in the lens gap-junction protein Connexin-50 (Cx50). CRISPR-based disruption of cx50 induces early eye loss in surface fish, and F2 laboratory crosses confirm genetic linkage between cx50 variants and eye size. Additional Cx50 mutations are present in independent cavefish populations and correlate with reduced eye size. Notably, variants in conserved regions of Cx50 also occur in other cave-dwelling fish and subterranean mammals, suggesting repeated evolutionary targeting of this gene. Introduction of the Caballo Moro mutation into mice causes cataracts and reduced eye and lens size, confirming its functional impact. Together, these findings identify the first SNP directly implicated in cavefish eye loss, demonstrate the power of natural hybrid populations to resolve the genetic basis of complex traits, and reveal Cx50 as a case of molecular convergence in vertebrate eye degeneration.

evolutionary biology↗

bioRxiv2024

Elevated DNA Damage without signs of aging in the short-sleeping Mexican Cavefish

Dysregulation of sleep has widespread health consequences and represents an enormous health burden. Short-sleeping individuals are predisposed to the effects of neurodegeneration, suggesting a critical role for sleep in the maintenance of neuronal health. While the effects of sleep on cellular function are not completely understood, growing evidence has identified an association between sleep loss and DNA damage, raising the possibility that sleep facilitates efficient DNA repair. The Mexican tetra fish, Astyanax mexicanus provides a model to investigate the evolutionary basis for changes in sleep and the consequences of sleep loss. Multiple cave-adapted populations of these fish have evolved to sleep for substantially less time compared to surface populations of the same species without identifiable impacts on healthspan or longevity. To investigate whether the evolved sleep loss is associated with DNA damage and cellular stress, we compared the DNA Damage Response (DDR) and oxidative stress levels between A. mexicanus populations. We measured markers of chronic sleep loss and discovered elevated levels of the DNA damage marker {gamma}H2AX in the brain, and increased oxidative stress in the gut of cavefish, consistent with chronic sleep deprivation. Notably, we found that acute UV-induced DNA damage elicited an increase in sleep in surface fish but not in cavefish. On a transcriptional level, only the surface fish activated the photoreactivation repair pathway following UV damage. These findings suggest a reduction of the DDR in cavefish compared to surface fish that coincides with elevated DNA damage in cavefish. To examine DDR pathways at a cellular level, we created an embryonic fibroblast cell line from the two populations of A. mexicanus. We observed that both the DDR and DNA repair were diminished in the cavefish cells, corroborating the in vivo findings and suggesting that the acute response to DNA damage is lost in cavefish. To investigate the long-term impact of these changes, we compared the transcriptome in the brain and gut of aged surface fish and cavefish. Strikingly, many genes that are differentially expressed between young and old surface fish do not transcriptionally vary by age in cavefish. Taken together, these findings suggest that cavefish have developed resilience to sleep loss, despite possessing cellular hallmarks of chronic sleep deprivation.

neuroscience↗

bioRxiv2022

Selection-driven trait loss in independently evolved cavefish populations

Predicting the outcome of evolution is a central goal of modern biology, yet, determining the relative contributions of deterministic events (i.e., selection) and stochastic events (i.e., drift and mutation) to the evolutionary process remains a major challenge. Systems where the same traits have evolved repeatedly provide natural replication that can be leveraged to study the predictability of molecular evolution and the genetic basis of adaptation. Although mutational screens in the laboratory have demonstrated that a diversity of genetic mutations can produce phenocopies of one another, in natural systems, similar genetic changes frequently underly the evolution of phenotypes across independent lineages. This suggests a substantial role for constraint and determinism in evolution and supports the notion that there may be characteristics which make certain mutations more likely to contribute to phenotypic evolution. Here we use large-scale whole genome resequencing in the Mexican tetra, Astyanax mexicanus, to demonstrate that selection has played a primary role in repeated evolution of both trait loss and trait enhancement across independent cave lineages. We identify candidate genes underlying repeated adaptation to caves and infer the mode of repeated evolution, revealing that selection on standing genetic variation and de novo mutations both contribute substantially to repeated adaptation. Finally, we show that genes with evidence of repeated evolution have significantly longer coding regions compared to the rest of the genome, and this effect is most pronounced in genes evolving convergently via independent mutations. Importantly, our findings provide the first empirical support for the hypothesis that genes with larger mutational targets are more likely to be the substrate of repeated evolution and indicate that features of the novel cave environment may impact the rate at which mutations occur.

evolutionary biology↗

bioRxiv2021

Hybridization underlies localized trait evolution in cavefish

Compared to selection on new mutations and standing genetic variation, the role of gene flow in generating adaptive genetic variation has been subject to much debate. Theory predicts that gene flow constrains adaptive evolution via natural selection by homogenizing allele frequencies among populations and introducing migrant alleles that may be locally maladaptive1. However, recent work has revealed that populations can diverge even when high levels of gene flow are present2-4 and that gene flow may play an underappreciated role in facilitating local adaptation by increasing the amount of genetic variation present for selection to act upon5-8. Here, we investigate how genetic variation introduced by gene flow contributes to adaptive evolution of complex traits using an emerging eco-evolutionary model system, the Mexican tetra (Astyanax mexicanus). The ancestral surface form of the Mexican tetra has repeatedly invaded and adapted to cave environments. The Chica cave is unique in that it contains several pool microenvironments inhabited by putative hybrids between surface and cave populations9, providing an opportunity to investigate the dynamics of complex trait evolution and gene flow on a local scale. Here we conduct high-resolution genomic mapping and analysis of eye morphology and pigmentation in fish from multiple pools within Chica cave. We demonstrate that hybridization between cave and surface populations contributes to highly localized variation in behavioral and morphological traits. Analysis of sleep and locomotor behaviors between individual pools within this cave revealed reduced sleep associated with an increase in ancestry derived from cave populations, suggesting pool-specific ecological differences may drive the highly-localized evolution of sleep and locomotor behaviors. Lastly, our analyses uncovered a compelling example of convergent evolution in a core circadian clock gene in multiple independent cavefish lineages and burrowing mammals, indicating a shared genetic mechanism underlying circadian disruption in subterranean vertebrates. Together, our results provide insight into the evolutionary mechanisms that promote adaptive genetic variation and the genetic basis of complex behavioral phenotypes involved in local adaptation.

evolutionary biology↗

bioRxiv2020

A chromosome level genome of Astyanax mexicanus surface fish for comparing population-specific genetic differences contributing to trait evolution.

Identifying the genetic factors that underlie complex traits is central to understanding the mechanistic underpinnings of evolution. In nature, adaptation to severe environmental change, such as encountered following colonization of caves, has dramatically altered genomes of species over varied time spans. Genomic sequencing approaches have identified mutations associated with troglomorphic trait evolution, but the functional impacts of these mutations remain poorly understood. The Mexican Tetra, Astyanax mexicanus, is abundant in the surface waters of northeastern Mexico, and also inhabits at least 30 different caves in the region. Cave-dwelling A. mexicanus morphs are well adapted to subterranean life and many populations appear to have evolved troglomorphic traits independently, while the surface-dwelling populations can be used as a proxy for the ancestral form. Here we present a high-resolution, chromosome-level surface fish genome, enabling the first genome-wide comparison between surface fish and cavefish populations. Using this resource, we performed quantitative trait locus (QTL) mapping analyses for pigmentation and eye size and found new candidate genes for eye loss such as dusp26. We used CRISPR gene editing in A. mexicanus to confirm the essential role of a gene within an eye size QTL, rx3, in eye formation. We also generated the first genome-wide evaluation of deletion variability that includes an analysis of the impact on protein-coding genes across cavefish populations to gain insight into this potential source of cave adaptation. The new surface fish genome reference now provides a more complete resource for comparative, functional, developmental and genetic studies of drastic trait differences within a species.Competing Interest StatementThe authors have declared no competing interest.View Full Text

genomics↗

bioRxiv2020

Rapture-ready darters: sequence capture outperforms whole genome data regardless of reference genome in Etheostoma

Researchers studying non-model organisms have an increasing number of methods available for generating genomic data. However, the applicability of different methods across species, as well as the effect of reference genome choice on population genomic inference, are still difficult to predict in many cases. We evaluated the impact of data type (whole-genome vs. reduced representation) and reference genome choice on data quality and on population genomic and phylogenomic inference across several species of darters (subfamily Etheostomatinae), a highly diverse radiation of freshwater fish. We generated a high-quality reference genome and developed a hybrid RADseq/sequence capture (Rapture) protocol for the Arkansas darter (Etheostoma cragini). Rapture data from 1900 individuals spanning four darter species showed recovery of most loci across darter species at high depth and consistent estimates of heterozygosity regardless of reference genome choice. Loci with baits spanning both sides of the restriction enzyme cut site performed especially well across species. For low-coverage whole-genome data, choice of reference genome affected read depth and inferred heterozygosity. For similar amounts of sequence data, Rapture performed better at identifying fine-scale genetic structure compared to whole-genome sequencing. Rapture loci also recovered an accurate phylogeny for the study species and demonstrated high phylogenetic informativeness across the evolutionary history of the genus Etheostoma. Low cost and high cross-species effectiveness regardless of reference genome suggest that Rapture and similar sequence capture methods may be worthwhile choices for studies of diverse species radiations.

genomics↗

bioRxiv2018

Agonistic character displacement of genetically based male color patterns across darters

A growing number of studies are demonstrating that interspecific male-male competitive interactions can promote trait evolution and contribute to speciation. Agonistic character displacement (ACD) occurs when selection to avoid maladaptive interspecific aggression leads to the evolution of agonistic signals and/or associated behavioral biases in sympatry. Here we test for a pattern consistent with ACD in male color pattern in darters (Percidae: Etheostoma). Despite the presence of traditional sex roles and sexual dimorphism, male color pattern has been shown to function in male-male competition in several darter species, rather than female mating preferences. A pattern consistent with divergent ACD in male behavioral biases has also been documented in darters. Males bias their aggression towards conspecific over heterospecific males in sympatry but not in allopatry. Here we use a common garden approach to show that differences in male color pattern among four closely related darter species are genetically based. We also demonstrate that male color pattern exhibits enhanced differences in sympatric compared to allopatric populations of two darter species. This study provides evidence that interspecific male-male aggressive interactions alone can promote elaborate male signal evolution both between and within species. We discuss the implications this has for male-driven ACD and cascade ACD.

evolutionary biology↗

bioRxiv2018

Hybridization and postzygotic isolation promote reinforcement of male mating preferences in a diverse group of fishes with traditional sex roles

Behavioral isolation is thought to arise early in speciation due to differential sexual and/or natural selection favoring different preferences and traits in different lineages. Alternatively, behavioral isolation can arise due to reinforcement favoring traits and preferences that prevent maladaptive hybridization. In darters, female preference for male coloration has been hypothesized to drive speciation, because behavioral isolation evolves before F1 inviability. However, as with many long-lived organisms, the fitness of second generation hybrids has not been assessed because raising animals to adulthood in the lab is challenging. Recently, reinforcement of male preferences has been implicated in darters because male preference for conspecific females is high in sympatry but absent in allopatry in multiple species pairs. The hypothesis that reinforcement accounts for behavioral isolation in sympatry assumes that hybridization and postzygotic isolation are present. Here, we used genomic and morphological data to demonstrate that hybridization is ongoing between orangethroat and rainbow darters and used hybrids collected from nature to measure postzygotic barriers across two hybrid generations. We observed sex ratio distortion in adult F1s and a dramatic reduction in backcross survival. Our findings indicate that selection to avoid hybridization promotes the evolution of male-driven behavioral isolation via reinforcement in this system.

evolutionary biology↗

bioRxiv2017

Egg viability decreases rapidly with time since ovulation in the rainbow darter: implications for the costs of choosiness

Egg viability in the rainbow darter Etheostoma caeruleum, a fish apparently lacking female mate choice, was found to decline rapidly after ovulation. We observed that the majority of a females clutch may fail to hatch if she is prevented from mating for as little as six hours. These data suggest that exercising female mate preferences may be selectively disfavoured in E. caeruleum due to the high cost of delaying mating.

animal behavior and cognition↗

bioRxiv2017

Male-driven reinforcement and cascade reinforcement in darters

Reinforcement can act in response to maladaptive hybridization by selecting for increased discrimination against heterospecifics mates in sympatry compared to allopatry (i.e., reproductive character displacement - RCD). Additionally, reinforcement can select for increased discrimination against heterospecifics in a fighting context in sympatry compared to allopatry (i.e., agonistic character displacement - ACD). Because it directly affects conspecific recognition traits (signals and/or preferences), reinforcement between two species in sympatry can incidentally cause behavioral isolation among populations within a species, termed cascade reinforcement. Here we demonstrate that a pattern consistent with male-driven RCD and ACD is present between two groups of darters (orangethroat darter clade Ceasia and rainbow darter Etheostoma caeruleum). Increased male discrimination against heterospecific females as mates and increased male discrimination against heterospecific males as competitors is present in sympatry. Furthermore, there is a pattern consistent with male-driven cascade RCD and cascade ACD within Ceasia. We found low levels of discrimination between two species of Ceasia that occur in allopatry from one another and in allopatry with E. caeruleum. This result contrasts that of a recent study which observed high levels of behavioral isolation between Ceasia species that occurred in sympatry with E. caeruleum. We suggest reinforcement between Ceasia and E. caeruleum in sympatry has led to the evolution of behavioral isolation between lineages within Ceasia that occur in sympatry with E. caeruleum but in allopatry with respect to one another (i.e., cascade reinforcement). This study demonstrates the ability of male behavior to simultaneously drive sympatric and allopatric speciation via reinforcement.

evolutionary biology↗