Biology subjects

Kelley, J. L.

Publications and source records attributed to Kelley, J. L..

At least 19 recordsLinked to original sources

bioRxiv2025

Tissue-specific plasticity of DNA methylation across intertidal microhabitats in juvenile mussels (Mytilus californianus)

Epigenetic modifications to DNA are proposed to underpin plastic responses to environmental change, and the manner in which DNA methylation contributes to plasticity likely differs among tissues. However, few studies have investigated tissue-specific DNA methylation responses to ecologically relevant environmental stressors in natural settings. Here, we used reduced representation bisulfite sequencing on foot and gill to examine the influence of in situ microhabitats on DNA methylation in juvenile California mussels (Mytilus californianus), a foundation species with widespread dispersal and little evidence of genetic population structure. We examined mussels from a one-month reciprocal transplant experiment between a cool, wave-exposed and a warm, wave-protected microhabitat. These manipulations, which were previously shown to alter juvenile mussels heat tolerance, led to significant and highly tissue-specific changes in CpG methylation, including within a number of genes with roles in stress response pathways. Differentially methylated genes were involved in processes including heat shock response, proteolysis, DNA repair, and temperature sensing. In gill, differentially methylated CpGs were more likely to occur in introns relative to other inter- and intragenic features. This study expands on previous research that examined environmentally driven shifts in DNA methylation by documenting plastic and tissue-specific changes in DNA methylation between microhabitats in a natural setting.

genomics↗

bioRxiv2025

Mitigating assembly and switch errors in phased genomes of polar fishes reveals haplotype diversity in copy number of antifreeze protein genes

Phased genomes and pangenomes are enhancing our understanding of genetic variation. Accurate phasing and assembly in repetitive regions of the genome remain challenging, however. Addressing this obstacle is crucial for studying structural genomic variation such as copy number variations (CNVs) common to repetitive regions. Polar fishes, for example, evolved repetitive tandem arrays of antifreeze protein (AFP) genes that facilitated adaptation to freezing and expanded in copy number in colder environments. AFP CNVs remain poorly characterized in polar fishes and may be illuminated by haplotype-aware approaches. We performed long-read sequencing of two polar fishes in the suborder Zoarcoidei and leveraged published long-read data to assemble phased genomes. We developed a workflow to measure haplotype diversity in CNV while controlling for misassembly and switch errors--a change from one parental haplotype to another in a contiguous assembly. We present gfa_parser, which computes and extracts all possible contiguous sequences for phased or primary assemblies from graphical fragment assembly files, and switch_error_screen, which flags potential switch errors. gfa_parser revealed that assembly uncertainty was ubiquitous across AFP array haplotypes and that standard processing of graphical fragment assemblies can bias measurement of haplotype CNVs. We detected no switch errors in AFP arrays. After controlling for misassembly and switch error, we detected haplotype diversity of AFP CNVs in all studied polar Zoarcoidei species and in 60% of AFP arrays. Intraindividual haplotype diversity spanned differences of 3-16 copies. Our workflow revealed intraspecific genomic diversity in zoarcoids that likely fueled evolution of AFP copy number across temperature.

genomics↗

bioRxiv2025

Drivers of genetic diversity across the marine tree of life

Why do some species have more genetic diversity than others? This question is one of the greatest remaining mysteries in evolutionary biology, yet we still know little about what factors predict genetic diversity among species. Efforts to quantify diversity or understand its distribution have been hampered by a lack of genomic data analyzed in a consistent way with statistical approaches that can move beyond the population level to generate species-wide estimates of genetic diversity. We address this critical gap by generating standardized estimates of genomic-level genetic diversity for 93 species sampled over 9,000 localities. Because marine species have evolved a strikingly diverse array of biological traits that have long been hypothesized to affect species-level genetic diversity, we focus our study on marine taxa. For each species, we aggregated biotic traits related to life history and abiotic features of the species range. We show that genetic diversity increases with species range extent and planktonic dispersal. We hypothesize that these traits increase a species ability to avoid or recover from bottlenecks, thereby maintaining genetic diversity. Our findings provide insights into how biotic and abiotic factors interact to shape genomic variation in the ocean, and offer a predictive framework for understanding marine biodiversity in the face of global change. Significance statementSpecies exhibit vast trait diversity that allows populations to persist. However, diversity in these traits -- e.g., how organisms reproduce, disperse, and feed -- is not easily linked to what is known of genomic diversity, even in well-studied organisms. We investigate a diverse assemblage of marine species to begin to build a predictive framework for how species traits drive genomic diversity across the worlds oceans. We find that species with larger geographic ranges have higher genomic diversity. More dispersive species also harbor higher diversity, suggesting that greater dispersal facilitates resilience to environmental change. As available datasets increase, our ability to understand fundamental links between trait and genetic diversity and how they shape species responses to environmental change will continue to improve.

evolutionary biology↗

bioRxiv2024

Temperature and Pressure Shaped the Evolution of Antifreeze Proteins in Polar and Deep Sea Zoarcoid Fishes

Antifreeze proteins (AFPs) have enabled teleost fishes to repeatedly colonize polar seas. Four AFP types have convergently evolved in several fish lineages. AFPs inhibit ice crystal growth and lower cellular freezing point. In lineages with AFPs, species inhabiting colder environments may possess more AFP copies. Elucidating how differences in AFP copy number evolve is challenging due to the genes tandem array structure and consequently poor resolution of these repetitive regions. Here we explore the evolution of type III AFPs (AFP III) in the globally distributed suborder Zoarcoidei, leveraging six new long-read genome assemblies. Zoarcoidei has fewer genomic resources relative to other polar fish clades while it is one of the few groups of fishes adapted to both the Arctic and Southern Oceans. Combining these new assemblies with additional long-read genomes available for Zoarcoidei, we conducted a comprehensive phylogenetic test of AFP III evolution and modeled the effects of thermal habitat and depth on AFP III gene family evolution. We confirm a single origin of AFP III via neofunctionalization of the enzyme sialic acid synthase B and show that AFP copies expanded under low temperature, but also decreased with depth, which reduces freezing point via pressure. Associations between the environment and AFP III copy number were driven by duplications of paralogs that were translocated out of the ancestral locus at which Zoarcoidei AFP arose. Our results reveal novel environmental effects on AFP evolution and demonstrate the value of high-quality genomic resources for studying how structural genomic variation shapes convergent adaptation.

evolutionary biology↗

bioRxiv2024

Recommendations for Population and Individual Diagnostic SNP Selection in Non-Model Species

Despite substantial reductions in the cost of sequencing over the last decade, genetic panels remain relevant due to their cost-effectiveness and flexibility across a variety of sample types. In particular, single nucleotide polymorphism (SNP) panels are increasingly favored for conservation applications. SNP panels are often used because of their adaptability, effectiveness with low-quality samples, and cost-efficiency for use in population monitoring and forensics. However, the selection of diagnostic SNPs for population assignment and individual identification can be challenging. The consequences of poor SNP selection are under-powered panels, inaccurate results, and monetary loss. Here, we develop a novel user-friendly SNP selection pipeline for population assignment and individual identification, mPCRselect. mPCRselect allows any researcher, who has sufficient SNP-level data, to design a successful and cost-effective SNP panel for species of conservation concern.

evolutionary biology↗

bioRxiv2024

Phylogenetic signal in primate tooth enamel proteins and its relevance for paleoproteomics

Ancient tooth enamel, and to some extent dentin and bone, contain characteristic peptides that persist for long periods of time. In particular, peptides from the enamel proteome (enamelome) have been used to reconstruct the phylogenetic relationships of fossil specimens and to estimate divergence times. However, the enamelome is based on only about 10 genes, whose protein products undergo fragmentation post mortem. Moreover, some of the enamelome genes are paralogous or may coevolve. This raises the question as to whether the enamelome provides enough information for reliable phylogenetic inference. We address these considerations on a selection of enamel-associated proteins that has been computationally predicted from genomic data from 232 primate species. We created multiple sequence alignments (MSAs) for each protein and estimated the evolutionary rate for each site and examined which sites overlap with the parts of the protein sequences that are typically isolated from fossils. Based on this, we simulated ancient data with different degrees of sequence fragmentation, followed by phylogenetic analysis. We compared these trees to a reference species tree. Up to a degree of fragmentation that is similar to that of fossil samples from 1-2 million years ago, the phylogenetic placements of most nodes at family level are consistent with the reference species tree. We found that the composition of the proteome influences the phylogenetic placement of Tarsiiformes. For the inference of molecular phylogenies based on paleoproteomic data, we recommend characterizing the evolution of the proteomes from the closest extant relatives to maximize the reliability of phylogenetic inference.

evolutionary biology↗

bioRxiv2023

Gene expression signatures of salinity transitions in Limia perugiae (Poeciliidae), with comparisons to other teleosts

Salinity gradients act as strong environmental barriers that limit the distribution of aquatic organisms. Changes in gene expression associated with transitions between freshwater and saltwater environments can provide insight into organismal responses to variation in salinity. We used RNA-sequencing (RNA-seq) to investigate genome-wide variation in gene expression between a hypersaline population and a freshwater population of the livebearing fish species Limia perugiae (Poeciliidae). Our analyses of gill gene expression revealed potential molecular mechanisms underlying salinity tolerance in this species, including the enrichment of genes involved in ion transport, maintenance of chemical homeostasis, and cell signaling in the hypersaline population. We also found differences in gene expression patterns associated with cell cycle and protein folding processes between the hypersaline and freshwater L. perugiae. Bidirectional freshwater-saltwater transitions have occurred repeatedly during the diversification of fishes, allowing for broad-scale examination of repeatable patterns in evolution. We compared transcriptomic variation in L. perugiae with other teleosts that have made freshwater-saltwater transitions to test for convergence in gene expression. Among the four distantly related population pairs from high- and low-salinity environments that we included in our analysis, we found only ten shared differentially expressed genes, indicating little evidence for convergence. However, we found that differentially expressed genes shared among three or more lineages were functionally enriched for ion transport and immune functioning. Overall, our results--in conjunction with other recent studies-- suggest that different genes are involved in salinity transitions across disparate lineages of teleost fishes.

physiology↗

bioRxiv2023

What does the fox (genome) say? A chromosome-level assembly for the gray fox (Urocyon cinereoargenteus)

Reference genome assemblies have been created from multiple lineages within the Canidae family, however, despite its phylogenetic relevance as a basal genus within the clade, there is currently no reference genome for the gray fox (Urocyon cinereoargenteus). Here, we present a chromosome-level assembly for the gray fox (U. cinereoargenteus), which represents the most contiguous, non-domestic canid reference genome available to date, with 90% of the genome contained in just 34 scaffolds and a contig N50 and scaffold N50 of 59.4 and 72.9 Megabases (Mb), respectively. Repeat analyses identified an increased number of simple repeats relative to other canids. Based on mitochondrial DNA, our Vermont sample clusters with other gray fox samples from the northeastern US and contains slightly lower levels of heterozygosity than gray foxes on the west coast of California. This new assembly lays the groundwork for future studies to describe past and present population dynamics, including the delineation of evolutionarily significant units of management relevance. Importantly, the phylogenetic position of Urocyon allows us to verify the loss of PRDM9 functionality in the basal canid lineage, confirming that pseudogenization occurred at least 10 million years ago.

genomics↗

bioRxiv2023

Whole genome approach to the structure and dynamics of Cacajao wild populations

Despite showing the greatest primate diversity on the planet, genomic studies on Amazonian primates show very little representation in the literature. With 48 geolocalized high coverage whole genomes from wild uakari monkeys, we present the first population-level study on platyrrhines using whole genome data. In a very restricted range of the Amazon rainforest, eight uakari species (Cacajao genus) have been described and categorized into bald and black uakaris, based on phenotypic and ecological differences. Despite a slight habitat overlap, we show that posterior to their split 0.92 Mya, bald and black uakaris have remained independent, without gene flow. Nowadays, these two groups present distinct genetic diversity and group-specific variation linked to pathogens. We propose differing hydrology patterns and effectiveness of geographic barriers have modulated the intra-group connectivity and structure of uakari populations. Beyond increasing their representation, with this work we explored the effects of the Amazon rainforests dynamism on platyrrhine species.

evolutionary biology↗

bioRxiv2022

Ghost admixture in eastern gorillas

Archaic admixture has had a significant impact on human evolution with multiple events across different clades, including from extinct hominins such as Neanderthals and Denisovans into modern humans. Within the great apes archaic admixture has been identified in chimpanzees and bonobos, but the possibility of such events has not been explored in other species. Here, we address this question using high-coverage whole genome sequences from all four extant gorilla subspecies, including six newly sequenced eastern gorillas from previously unsampled geographic regions. Using Approximate Bayesian Computation (ABC) with neural networks to model the demographic history of gorillas, we find a signature of admixture from an archaic ghost lineage into the common ancestor of eastern gorillas, but not western gorillas. We infer that up to 3% of the genome of these individuals is introgressed from an archaic lineage that diverged more than 3 million years ago from the common ancestor of all extant gorillas. This introgression event took place before the split of mountain and eastern lowland gorillas, likely more than 40 thousand years ago, and may have influenced perception of bitter taste in eastern gorillas. When comparing the introgression landscapes of gorillas, humans and bonobos, we find a consistent depletion of introgressed fragments on the X chromosome across these species. However, depletion in protein-coding content is not detectable in eastern gorillas, possibly as a consequence of stronger genetic drift in this species.

evolutionary biology↗

bioRxiv2022

A beary good genome: Haplotype-resolved, chromosome-level assembly of the brown bear (Ursus arctos)

The brown bear (Ursus arctos) is the second largest and most widespread extant terrestrial carnivore on Earth and has recently emerged as a medical model for human metabolic diseases. Here, we report a fully-phased chromosome-level assembly of a male North American brown bear built by combining Pacific Biosciences (PacBio) HiFi data and publicly available Hi-C data. The final genome size is 2.47 Gigabases (Gb) with a scaffold and contig N50 length of 70.08 and 43.94 Mb, respectively. BUSCO analysis revealed that 94.5% of single-copy orthologs from mammalia were present in the genome (the highest of any ursid genome to date). Repetitive elements accounted for 44.48% of the genome and a total of 20,480 protein coding genes were identified. Based on whole genome alignment, the brown bear is highly syntenic with the polar bear, and our phylogenetic analysis of 7,246 single-copy BUSCOs supports the currently proposed species tree for Ursidae. This highly contiguous genome assembly will support future research on both the evolutionary history of the bear family and the physiological mechanisms behind hibernation, the latter of which has broad medical implications. SignificanceBrown bears (Ursus arctos) are the most widespread, large terrestrial carnivore on the planet and represent an interesting example of speciation through hybridization, as well as a medical model for sedentary lifestyle-related disease. Although a previous genome for a brown bear has been published, the reported contig N50 was low (only [~]530 kb), despite being scaffolded into putative chromosomes. Genomes of this quality limit the accuracy of analyses which rely on long contiguous stretches of the genome to be assembled (such as with many demographic analyses) as well as attempts at connecting genotype to phenotype (such as in association analyses). In order to support studies on both the complex hybridization history of the brown bear and investigations into medically-relevant phenotypes, we generated a fully-phased, chromosome-level assembly from a male grizzly bear. The genome has a total size of 2.47 Gb and 90% of the genome is contained in 36 scaffolds, roughly corresponding to one autosome per scaffold. This high-quality genome will enable studies across a variety of disciplines, including conservation, evolution, and medicine.

genomics↗

bioRxiv2022

Repetitive elements in the era of biodiversity genomics: insights from 600+ insect genomes

Repetitive elements (REs) are integral to the composition, structure, and function of eukaryotic genomes, yet remain understudied in most taxonomic groups. We investigated REs across 601 insect species and report wide variation in REs dynamics across groups. Analysis of associations between REs and protein-coding genes revealed dynamic evolution at the interface between REs and coding regions across insects, including notably elevated RE-gene associations in lineages with abundant long interspersed nuclear elements (LINEs). We leveraged this large, empirical data set to quantify impacts of long-read technology on RE detection and investigate fundamental challenges to RE annotation in diverse groups. In long-read assemblies we detected [~]36% more REs than short-read assemblies, with long terminal repeats (LTRs) showing 162% increased detection, while DNA transposons and LINEs showed less respective technology-related bias. In most insect lineages, 25-85% of repetitive sequences were "unclassified" following automated annotation, compared to only [~]13% in Drosophila species. Although the diversity of available insect genomes has rapidly expanded, we show the rate of community contributions to RE databases has not kept pace, preventing efficient annotation and high-resolution study of REs in most groups. We highlight the tremendous opportunity and need for the biodiversity genomics field to embrace REs and suggest collective steps for making progress towards this goal.

genomics↗

bioRxiv2022

Hibernation shows no apparent effect on germline mutation rates in grizzly bears

A male mutation bias is observed across vertebrates, and, where data are available, this bias is accompanied by increased per-generation mutation rates with parental age. While continuing mitotic cell division in the male germline post-puberty has been proposed as the major cellular mechanism underlying both patterns, little direct evidence for this role has been found. Understanding the evolution of the per-generation mutation rate among species requires that we identify the molecular mechanisms that change between species. Here, we study the per-generation mutation rate in an extended pedigree of the brown (grizzly) bear, Ursus arctos horribilis. Brown bears hibernate for one-third of the year, a period during which spermatogenesis slows or stops altogether. The cessation of spermatogenesis is predicted to lessen the male mutation bias and to lower the per-generation mutation rate in this species. However, using whole-genome sequencing, we find that both male bias and per-generation mutation rates are the same as expected for a non-hibernating species. We also carry out a phylogenetic comparison of substitution rates along the lineage leading to brown bear and panda (a non-hibernating species) and find no slowing of the substitution rate in the hibernator. Our results contribute to accumulating evidence that suggests that male germline cell division is not the major determinant of mutation rates and mutation biases. The results also provide a quantitative basis for improved estimates of the timing of carnivore evolution.

evolutionary biology↗

bioRxiv2021

Ecology drives the degree of convergence in the gene expression of extremophile fishes

Convergent evolution, where independent lineages evolve similar traits when adapting to similar habitats, is a common phenomenon and testament to the repeatability of evolutionary processes. Still, non-convergence is also common, and a major question is whether apparently idiosyncratic, lineage-specific evolutionary changes are reflective of chance events inherent to evolutionary processes, or whether they are also influenced by deterministic genetic or ecological factors. To address this question, we quantified the degree of convergence in genome-wide patterns of gene expression across lineages of livebearing fishes (family Poeciliidae) that span 40 million years of evolution and have colonized extreme environments in the form of toxic, hydrogen-sulfide-rich springs. We specifically asked whether the degree of convergence across lineage pairs was related to their phylogenetic relatedness or the ecological similarity of the habitats they inhabit. Using phylogenetic comparative analyses, we showed that the degree of convergence was highly variable across lineage pairs residing in sulfide springs. While closely related lineages did not exhibit higher degrees of convergence than distantly related ones, we uncovered a strong relationship between degree of convergence and ecological similarity. Our results indicate that variation in the degree of convergence is not merely noise associated with evolutionary contingency. Rather, cryptic environmental variation that is frequently ignored when we employ reductionist approaches can significantly contribute to adaptive evolution. This study highlights the importance of multivariate approaches that capture the complexities of both selective regimes and organismal design when assessing the roles of determinism and contingency in evolution. Significance StatementWhen different species adapt to similar environmental conditions, we frequently observe a mix between shared (convergent) and lineage-specific (nonconvergent) evolutionary changes. Shared changes provide evidence for the repeatability and predictability of evolution. However, it remains unclear whether lineage-specific changes are caused by random forces that limit the predictability of evolution, or whether they reflect deterministic processes shaped by unidentified genetic and environmental factors. By analyzing patterns of gene expression across fishes in extreme environments, we show that the degree of convergence between lineages is related to ecology, indicating that lineage-specific evolutionary changes are not just noise caused by random processes. Thus, acknowledging the complexity of nature in empirical research is critical if we want to predict evolution.

evolutionary biology↗

bioRxiv2021

Pathways to polar adaptation in fishes revealed by long-read sequencing

Long-read sequencing is driving a new reality for genome science where highly contiguous assemblies can be produced efficiently with modest resources. Genome assemblies from long-read sequences are particularly exciting for understanding the evolution of complex genomic regions that are often difficult to assemble. In this study, we leveraged long-read sequencing data to generate a high-quality genome assembly for an Antarctic eelpout, Opthalmolycus amberensis, the first for the globally distributed family Zoarcidae. We used this assembly to understand how O. amberensis has adapted to the harsh Southern Ocean and compared it to another group of Antarctic fishes: the notothenioids. We showed that selection has largely acted on different targets in eelpouts relative to notothenioids. However, we did find some overlap; in both groups, genes involved in membrane structure, thermal tolerance, and vision have evidence of selection. We found evidence for historical shifts of transposable element activity in O. amberensis and other polar fishes, perhaps reflecting a response to environmental change. We were specifically interested in the evolution of two complex genomic loci known to underlie key adaptations to polar seas: hemoglobin and antifreeze proteins (AFPs). We observed unique evolution of the hemoglobin MN cluster in eelpouts and related fishes in the suborder Zoarcoidei relative to other Perciformes. For AFPs, we identified the first species in the suborder with no evidence of afpIII sequences (Cebidichthys violaceus) in the genomic region where they are found in all other Zoarcoidei, potentially reflecting a lineage-specific loss of this cluster. Beyond polar fishes, our results highlight the power of long-read sequencing to understand genome evolution.

genomics↗

bioRxiv2021

Towards a genome sequence for every animal: where are we now?

In less than 25 years, the field of animal genome science has transformed from a discipline seeking its first glimpses into genome sequences across the Tree of Life to a global enterprise with ambitions to sequence genomes for all of Earths eukaryotic diversity (1). As the field rapidly moves forward, it is important to take stock of the progress that has been made to best inform the disciplines future. In this Perspective, we provide a contemporary, quantitative overview of animal genome sequencing. We identified the best available genome assemblies on GenBank, the worlds most extensive genetic database, for 3,278 unique animal species across 24 phyla. We assessed taxonomic representation, assembly quality, and annotation status for major clades. We show that while tremendous taxonomic progress has occurred, stark disparities in genomic representation exist, highlighted by a systemic overrepresentation of vertebrates and underrepresentation of arthropods. In terms of assembly quality, long-read sequencing has dramatically improved contiguity, whereas gene annotations are available for just 34.3% of taxa. Furthermore, we show that animal genome science has diversified in recent years with an ever-expanding pool of researchers participating. However, the field still appears to be dominated by institutions in the Global North, which have been listed as the submitting institution for 77% of all assemblies. We conclude by offering recommendations for how we can collectively improve genomic resource availability and value while also broadening global representation. Significance statementThe field of animal genome science is rapidly developing, and efforts are underway to sequence genomes for all of Earths eukaryotic biodiversity. Here, we provide an overview of animal genome sequencing, with emphases on taxonomic representation, assembly quality, and geographic representation. We show that while a staggering 3,278 unique animal species have had their genomes sequenced, massive disparities exist in terms of the taxonomic groups receiving attention, the quality of the resources being produced, and the institutions driving the field. We highlight areas where improvements can be made, notably by continuing to increase the quality of genome assemblies, including by improving metadata and voucher specimen associations, and actively developing meaningful collaborations between researchers form the Global North and South.

genomics↗

bioRxiv2021

Long-read isoform sequencing reveals tissue-specific isoform expression between active and hibernating brown bears (Ursus arctos)

Understanding hibernation in brown bears (Ursus arctos) can provide insight into many human diseases. During hibernation, brown bears experience states of insulin resistance, physical inactivity, extreme bradycardia, obesity, and the absence of urine production. These states closely mimic human diseases such as type 2 diabetes, muscle atrophy, renal and heart failure, cachexia, and obesity. The reversibility of these states from hibernation to active season allows for the identification of novel mediators with possible therapeutic value for humans. Recent studies have identified genes and pathways that are differentially expressed between active and hibernation seasons. However, little is known about the role of differential expression of gene isoforms on hibernation physiology. To identify both distinct and novel mRNA isoforms, we performed full-length RNA-sequencing (Iso-Seq) on three tissue types from three individuals sampled during both active and hibernation seasons. We combined the long-read data with the reference annotation for an improved transcriptome and mapped RNA-seq data from six individuals to the improved transcriptome to quantify differential isoform usage between tissues and seasons. We identified differentially expressed isoforms in all study tissues and showed that adipose has a high level of differential isoform usage with isoform switching, regardless of whether the genes were differentially expressed. Our analyses provide a comprehensive evaluation of isoform usage between active and hibernation states, revealing that differential isoform usage, even in the absence of differential gene expression, is an important mechanism for modulating genes during hibernation. These findings demonstrate the value of isoform expression studies and will serve as the basis for deeper exploration into hibernation biology.

genomics↗

bioRxiv2021

Convergent adaptation and ecological speciation result from unique genomic mechanisms in sympatric extremophile fishes

The evolution of independent lineages along replicated environmental gradients frequently results in convergent adaptation, yet the degree to which convergence is present across multiple levels of biological organization is often unclear. Additionally, inherent biases associated with shared ancestry and variation in selective regimes across geographic replicates often pose challenges for confidently identifying patterns of convergence. We investigated a system in which three species of poeciliid fishes sympatrically occur in a toxic spring rich in hydrogen sulfide (H2S) and an adjacent nonsulfidic stream to examine patterns of adaptive evolution across levels of biological organization. We found convergence in morphological and physiological traits and genome-wide patterns of gene expression among all three species. In addition, there were shared signatures of selection on genes encoding H2S toxicity targets in the mitochondrial genomes of each species. However, analyses of nuclear genomes revealed neither evidence for substantial genomic islands of divergence around genes involved in H2S toxicity and detoxification nor substantial congruence of strongly differentiated regions across population pairs. These non-convergent, heterogenous patterns of genomic divergence may indicate that sulfide tolerance is highly polygenic, with shared allele frequency shifts present at many loci with small effects along the genome. Alternatively, H2S tolerance may involve substantial genetic redundancy, with non-convergent lineage-specific variation at multiple loci along the genome underpinning similar changes in phenotypes and gene expression. Overall, we demonstrate variability in the extent of convergence across organizational levels and highlight the challenges of linking patterns of convergence across scales.

evolutionary biology↗