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bioRxiv2019

Ecological specificity of the metagenome in a set of lower termite species supports contribution of the microbiome to adaptation of the host

BackgroundElucidating the interplay between hosts and their microbiomes in ecological adaptation has become a central theme in evolutionary biology. A textbook example of microbiome-mediated adaptation is the adaptation of lower termites to a wood-based diet, as they depend on their gut microbiome to digest wood. Lower termites have further adapted to different life types. Termites of the wood-dwelling life type never leave their nests and feed on a uniform diet. Termites of the foraging life type forage for food outside the nest and have access to other nutrients. Here we sought to investigate whether the microbiome that is involved in food substrate breakdown and nutrient acquisition might contribute to adaptation to these ecological differences. We reasoned that this should leave ecological imprints on the microbiome.\n\nResultsWe investigated the protist and bacterial microbiomes of a total of 29 replicate colonies from five termite species, covering both life types, using metagenomic shotgun sequencing. The microbiome of wood-dwelling species with a uniform wood diet was enriched for genes involved in lignocellulose degradation. Furthermore, metagenomic patterns suggest that the microbiome of wood-dwelling species relied primarily on direct fixation of atmospheric nitrogen, while the microbiome of foraging species entailed the necessary pathways to utilize nitrogen in the form of nitrate for example from soil.\n\nConclusionOur findings are consistent with the notion that the microbiome of wood-dwelling species bears an imprint of its specialization on degrading a uniform wood diet, while the microbiome of the foraging species might reflect its adaption to access growth limiting nutrients from more diverse sources. This supports the idea that specific subsets of functions encoded by the microbiome can contribute to host adaptation.

evolutionary biology↗
bioRxiv2025

The Driving W Hypothesis for Low Within-Population Mitochondrial DNA Diversity and Between-Population Mitochondrial Capture

The fields of evolutionary biology, molecular ecology, genetics, and taxonomy have been profoundly influenced by studies of variation in mitochondrial DNA (mtDNA), yet there are often surprising differences between mtDNA and nuclear DNA in the within- and between-population relationships that they display. Here I articulate and evaluate a hypothesis that may explain many of the cases in which mtDNA shows little within-population variation and recent movement between populations. Many taxonomic groups (e.g., birds, butterflies and moths; most snakes; some amphibians, fish, and plants) have sex chromosome systems in which females are heterogametic (i.e., ZW females and ZZ males). If a W chromosome undergoes a mutation that gives it a transmission advantage in getting into the one egg produced by female meiosis, it will tend to cause a female-biased sex ratio in the offspring of females that carry that driving W chromosome. This sex ratio bias increases the frequency of the driving W in relation to the non-driving W in the next generation. In the great majority of species in which mitochondria are inherited matrilineally, the spread of the driving W through the population will carry along the particular mitochondrial genome that happens to be associated with the driving W. I summarize evidence in support of the seven components of this W-mtDNA Drive Hypothesis and present simulations and mathematical formulae showing that W drivers spread much more rapidly than equivalent-strength Z or autosomal drivers. Suppressors of W drive spread at a vastly lower rate. I conclude that many cases of low within-population mitochondrial diversity and mitochondrial transfer between species might be explained by the spread of driving W chromosomes.

evolutionary biology↗
bioRxiv2019

Familiar neighbors, but not relatives, enhance fitness in a territorial mammal

SummaryOne of the outstanding questions in evolutionary biology is the extent to which mutually beneficial interactions and kin-selection can facilitate the evolution of cooperation by mitigating conflict between interacting organisms. The indirect fitness benefits gained from associating with kin are an important pathway to conflict resolution [1], but conflict can also be resolved if individuals gain direct benefits from cooperating with one another (e.g. mutualism or reciprocity) [2]. Owing to the kin-structured nature of many animal societies, it has been difficult for previous research to assess the relative importance of these mechanisms [3-5]. However, one area that might allow for the relative roles of kin-selection and mutualistic benefits to be disentangled is in the resolution of conflict over territorial space [6]. While much research has focused on group-living species, the question of how cooperation can first be favoured in solitary, territorial species remains a key question. Using 22 years of data from a population of North American red squirrels, we assessed how kinship and familiarity with neighbours affected fitness in a territorial mammal. While living near kin did not enhance fitness, familiarity with neighbours increased survival and annual reproductive success. These fitness benefits were strong enough to compensate for the effects of aging later in life, with potential consequences for the evolution of senescence. We suggest that such substantial fitness benefits provide the opportunity for the evolution of cooperation between adversarial neighbours, offering insight into the role that mutually beneficial behaviours might play in facilitating and stabilizing social systems. Graphical Abstract O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

evolutionary biology↗
bioRxiv2017

Using Connectivity To Identify Climatic Drivers Of Local Adaptation

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100034). Despite being able to conclusively demonstrate local adaptation, we are still often unable to objectively determine the climatic drivers of local adaptation. Given the rapid rate of global change, understanding the climatic drivers of local adaptation is vital. Not only will this tell us which climate axes matter most to population fitness, but such knowledge is critical to inform management strategies such as translocation and targeted gene flow. While simple assessments of geographic trait variation are useful, geographic variation (and its associations with environment) may represent plastic, rather than evolved, differences. Additionally, the vast number of trait-environment combinations makes it difficult to determine which aspects of the environment populations adapt to. Here we argue that by incorporating a measure of landscape connectivity as a proxy for gene flow, we can differentiate between trait-environment relationships underpinned by genetic differences versus those that reflect phenotypic plasticity. By doing so, we can rapidly shorten the list of trait-environment combinations that may be of adaptive significance. We demonstrate how this reasoning can be applied using data on geographic trait variation in a lizard species from Australia's Wet Tropics rainforest. Our analysis reveals an overwhelming signal of local adaptation for the traits and environmental variables we investigated. Our analysis also allows us to rank environmental variables by the degree to which they appear to be driving local adaptation. Although encouraging, methodological issues remain: we point to these issue in the hope that the community can rapidly hone the methods we sketch here. The promise is a rapid and general approach to identifying the environmental drivers of local adaptation.

evolutionary biology↗
bioRxiv2023

Do color polymorphisms reflect pollinator shifts?: Integrating floral traits as signals to a novel pollinator to understand species divergence

Understanding how evolution proceeds from molecules to organisms to interactions is critical for evolutionary biology and requires integrative studies that span biological levels. By linking phenotypic changes with associated genes and fitness implications, we gain insight on the repeatability of evolution and how adaptive walks move organisms between fitness peaks, which remains poorly understood at intermediate stages, e.g. potential fitness valleys. Floral trait evolution can proceed rapidly, confer reproductive isolation, and provides numerous examples of convergent evolution associated with pollinator guilds. Within the monkeyflowers (Mimulus sect. Erythranthe), intraspecific shifts to yellow flowers within red hummingbird-pollinated species have arisen at least twice and may represent incipient shifts between optima of pollinator adaptation. Here, we compare two natural yellow-flowered forms of M. cardinalis and M. verbenaceus to their red conspecifics in floral phenotypes, biochemistry, transcriptomic and genomic variation, and interactions with pollinators. We find convergent evolution in the adaptive walks of yellow morphs in both species, with consistent changes in traits of large effect (floral pigments and associated gene expression), which result in strong preference for yellow flowers by bumblebees. Shifts in additional traits (scent emissions and floral opening size) are also consistent with bee pollination, which may represent smaller-effect steps in an ongoing walk from hummingbird to bee pollination. By examining intraspecific variation representing incipient pollinator shifts in two related species, this work elucidates how adaptive walks proceed at early stages by highlighting how convergent large effect mutations (floral color) may drive pollinator attraction, preceding smaller effect changes controlling pollinator fit and reward access. This work integrates phenotypic, biochemical, genomic, and behavioral evidence to shed light on how repeated steps in adaptive walks to new fitness optima may impact reproductive isolation and incipient speciation via convergent evolution.

evolutionary biology↗
bioRxiv2025

Fluctuating selection breaks Hamilton's rule for the evolution of altruism

Altruistic behaviours, those that benefit recipients at a cost to donors, have long posed a puzzle in evolutionary biology and sociobiology. Established theories, such as kin selection, group selection, and reciprocal altruism, explain altruism via assortment mechanisms that depend on preferential interactions among altruists to ensure a higher average payoff than selfish individuals. Hamiltons rule defines the minimum level of such assortative interactions required for altruism to evolve. However, in populations with limited growth, increased competition can erode the selective advantage of altruism and thus require more stringent Hamiltons rule. Here, we propose a fundamentally different mechanism: fluctuating selection driven by increased competition due to added social benefits of altruism in populations with limited carrying capacity. Under fluctuating selection, altruists can invade a selfish population without the need of assortment mechanisms and outcompete selfish individuals through a transient phase, even when the cost of altruism exceeds its direct benefit. Classical invasion analysis, which compares the long-term growth rates of rare altruistic mutants and resident selfish individuals, fails in our model because both strategies exhibit zero long-term growth. Instead, we show that altruism can invade when its short-term, time-averaging growth rate exceeds that of selfish individuals, which necessitates a prolonged transient phase. This invasion is enabled by payoff-regulated density dependence, which captures the dynamic interplay between payoff and density on fitness under fluctuating selection. Our findings challenge the necessity of Hamiltons rule and show that genuine altruism, with less average payoff than selfish individuals, even extremely self-sacrificial, can emerge under natural selection. This suggests that altruism may arise not from preferential interaction, but as an adaptive response to population fluctuations in constrained environments, providing an alternative paradigm for understanding the evolution of altruistic behaviour.

evolutionary biology↗
bioRxiv2023

Scattered differentiation of unlinked loci across the genome underlines ecological divergence of the selfing grass Brachypodium stacei

Ecological divergence without geographic isolation, as an early speciation process that may lead finally to reproductive isolation through natural selection, remains one of the most interesting issues in evolutionary biology. However, the patterns of the underlying genetic divergences across the genome vary between different groups. Here we report that Brachypodium stacei, an inbreeding grass species, has been involved in sympatric ecological divergence without geographic isolation. Genomic, transcriptomic, and metabolomic analyses suggest that diploid B. stacei diverged sympatrically in two slopes with contrasting biomes at Evolution Canyon I (ECI), Mount Carmel, Israel, where gene flow has continued freely but reduced with the time. This ecological divergence involved the scattered divergence of many unlinked loci across the total genome that include both coding and non-coding regions. We also identified significantly differential expressions of ABA signaling pathway genes, and contrasting metabolome composition between the arid-vs forest-adapted B. stacei ECI populations. These results suggest that many small loci involved in environmental responses act additively to account for the ecological usages of this species in contrasted environments with gene flow. SignificanceEcological divergence provides evidence for the origin of species through natural selection that has governed evolutionists attention since Darwin. In this study, we present multiple-omics analyses of two plant populations growing sympatrically in contrasted environments and revealed their distinct differentiation across all examined data. These two populations share the most recent ancestor compared with other populations and their divergence started in the early Holocene. We revealed that gene flow had continued but with a progressive reduction over time. The genetic divergences are scattered across the total genome involving many unlinked coding and non-coding regions. These findings highlight the significance of natural selection in the ecological divergence that may finally lead to species formation without geographic isolation.

evolutionary biology↗
bioRxiv2015

Genomic analysis reveals major determinants of cis-regulatory variation in Capsella grandiflora

Understanding the causes of cis-regulatory variation is a long-standing aim in evolutionary biology. Although cis-regulatory variation has long been considered important for adaptation, we still have a limited understanding of the selective importance and genomic determinants of standing cis-regulatory variation. To address these questions, we studied the prevalence, genomic determinants and selective forces shaping cis-regulatory variation in the outcrossing plant Capsella grandiflora. We first identified a set of 1,010 genes with common cis-regulatory variation using analyses of allele-specific expression (ASE). Population genomic analyses of whole-genome sequences from 32 individuals showed that genes with common cis-regulatory variation are 1) under weaker purifying selection and 2) undergo less frequent positive selection than other genes. We further identified genomic determinants of cis-regulatory variation. Gene-body methylation (gbM) was a major factor constraining cis-regulatory variation, whereas presence of nearby TEs and tissue specificity of expression increased the odds of ASE. Our results suggest that most common cis-regulatory variation in C. grandiflora is under weak purifying selection, and that gene-specific functional constraints are more important for the maintenance of cis-regulatory variation than genome-scale variation in the intensity of selection. Our results agree with previous findings that suggest TE silencing affects nearby gene expression, and provide novel evidence for a link between gbM and cis-regulatory constraint, possibly reflecting greater dosage-sensitivity of body-methylated genes. Given the extensive conservation of gene-body methylation in flowering plants, this suggests that gene-body methylation could be an important predictor of cis-regulatory variation in a wide range of plant species.

Evolutionary Biology↗
bioRxiv2018

Linking micro and macroevolution in the presence of migration

1. The process of speciation is of key importance in evolutionary biology because it shapes macroevolutionary patterns. This process starts at the microevolutionary level, for instance, when two subpopulations evolve towards different phenotypic optima. The speed at which these optima are reached is controlled by the degree of stabilising selection, which pushes a mean trait towards an optimum within subpopulations, and ongoing migration that pulls the mean phenotype away from that optimum. Traditionally, macro phenotypic evolution with selection has been modelled by Ornstein-Uhlenbeck (OU) processes, but these models have ignored the role of migration within species.\n\n2. Here, our goal is to reconcile the processes of micro and macroevolution by modelling migration during speciation. More precisely, we introduce an OU model where migration happens between two subpopulations within a branch of a phylogeny and this migration decreases over time as it happens during speciation. We then use this model to study the evolution of trait means along a phylogeny, as well as the way phenotypic disparity between species changes with successive epochs.\n\n3. We show that ignoring the effect of migration in sampled time-series data leads to a significant underestimation of the selective forces acting upon it. We also show that migration decreases the expected phenotypic disparity between species and we show the effect of migration in the particular case of niche filling. We further introduce a method to jointly estimate selection and migration from time-series data.\n\n4. Our model extends standard results of interactions selection-migration in a microevolutionary time frame across multiple speciation events at a macroevolutionary scale. Our results further proof that not accounting for gene flow has important consequences in inferences at both the micro and macroevolutionary scale.

evolutionary biology↗
bioRxiv2017

Mutation supply and the repeatability of selection for antibiotic resistance

Whether evolution can be predicted is a key question in evolutionary biology. Here we set out to better understand the repeatability of evolution, which is a necessary condition for predictability. We explored experimentally the effect of mutation supply and the strength of selective pressure on the repeatability of selection from standing genetic variation. Different sizes of mutant libraries of an antibiotic resistance gene, TEM-1 {beta}-lactamase in Escherichia coli, were subjected to different antibiotic concentrations. We determined whether populations went extinct or survived, and sequenced the TEM gene of the surviving populations. The distribution of mutations per allele in our mutant libraries--generated by error-prone PCR--followed a Poisson distribution. Extinction patterns could be explained by a simple stochastic model that assumed the sampling of beneficial mutations was key for survival. In most surviving populations, alleles containing at least one known large-effect beneficial mutation were present. These genotype data also support a model which only invokes sampling effects to describe the occurrence of alleles containing large-effect driver mutations. Hence, evolution is largely predictable given cursory knowledge of mutational fitness effects, the mutation rate and population size. There were no clear trends in the repeatability of selected mutants when we considered all mutations present. However, when only known large-effect mutations were considered, the outcome of selection is less repeatable for large libraries, in contrast to expectations. Furthermore, we show experimentally that alleles carrying multiple mutations selected from large libraries confer higher resistance levels relative to alleles with only a known large-effect mutation, suggesting that the scarcity of high-resistance alleles carrying multiple mutations may contribute to the decrease in repeatability at large library sizes.

evolutionary biology↗
bioRxiv2024

Variations and predictability of epistasis on an intragenic fitness landscape.

How epistasis hinders or facilitates movement on fitness landscapes has been a longstanding question in evolutionary biology. High-throughput experiments have revealed that, despite their idiosyncratic nature, epistatic interactions can exhibit reproducible global statistical patterns. Recently, Papkou et al. constructed a fitness landscape for a 9-base pair region of the folA gene in Escherichia coli, which encodes dihydrofolate reductase (DHFR), and showed that this landscape is both rugged and highly navigable. Here, we analyze this landscape to address two questions: How does the nature of epistasis between two mutations change with genetic background? and How predictable is epistasis within a gene? We find that epistasis is "fluid": higher-order interactions cause the relationship between two mutations to shift strongly across genetic backgrounds. Mutations fall into two distinct categories: a small subset exhibit strong global epistasis, while the majority do not. Nonetheless, we find that the distribution of fitness effects (DFE) of a genotype is highly predictable from its fitness. These findings provide a gene-level perspective on how epistasis operates, revealing both its unpredictability and its statistical regularities, and offer a framework for predicting mutational effects from high-dimensional fitness landscapes. Significance Statement.The effect of a mutation on fitness depends on the genome in which it occurs, a phenomenon known as epistasis. Epistasis makes evolution difficult to predict, but recent work has uncovered statistical regularities in how it manifests. Using a fitness landscape of [~]260,000 variants of an E. coli gene, we show that higher-order interactions make pair-wise epistasis "fluid": the relationship between two mutations changes with genetic background. We also find that epistasis is "binary" - a small subset of mutations exhibits strong global statistical patterns, while most do not. These findings reveal new principles of how epistasis shapes protein evolution and, ultimately, organismal adaptation.

evolutionary biology↗
bioRxiv2026

The influence of incompatibilities and heterosis on hybrid population genetics

A long-standing question in evolutionary biology is: Under what circumstances can speciation occur despite hybridisation or because of hybridisation? Some models of hybrid incompatibilities predict that speciation can occur even in the presence of gene flow and strong selection against hybrids, an outcome also influenced by genetic contributions from parental species and genetic architecture. On the other hand, empirical work has shown that heterosis can counteract the effect of incompatibilities, hindering the speciation process. Theoretical models that simultaneously consider the positive and negative impacts of hybridisation on fitness remain scarce, raising questions about the effects of hybrid incompatibilities in the presence of heterosis. To address this question, we study how (Bateson)-Dobzhansky-Muller incompatibilities (BDMIs) interact with overdominant mutations in a two-locus population genetics model of an isolated hybrid population. We find that the strength of overdominance relative to incompatibilities determines the long-term genetic composition of the hybrid population. We show that high recombination exposes incompatibilities to selection and reduces the frequency of derived alleles in the hybrid population, limiting the strength of BDMIs that can be maintained by the balance with overdominance. We also show how neutral variation is affected by the strength of selection and the recombination rate between incompatible loci, generating patterns that include an increase in local variation resembling associative overdominance, or a reduction resembling background selection. Such variation of neutral variation, particularly at intermediate distances from BDMI loci, can generate peaks or troughs of diversity that are explained by the recombination rate between BDMI loci, and initial proportions of admixture between parental populations. Our work demonstrates how the genomic conflict caused by the interplay of overdominance and hybrid incompatibilities, recombination, and parental contributions, shape the genome of an isolated hybrid population.

evolutionary biology↗
bioRxiv2017

Speciation in sympatry with ongoing secondary gene flow and an olfactory trigger in a radiation of Cameroon cichlids

Whether speciation can happen in the absence of geographical barriers and if so, under which conditions, is a fundamental question in our understanding of the evolution of new species. Among candidates for sympatric speciation, Cameroon crater lake cichlid radiations have been considered the most compelling. However, it was recently shown that a more complex scenario than a single colonization followed by isolation underlies these radiations. Here, we perform a detailed investigation of the speciation history of a radiation of Coptodon cichlids from Lake Ejagham using whole-genome sequencing data. The existence of the Lake Ejagham Coptodon radiation is remarkable since this 0.5 km2 lake offers limited scope for divergence across a shallow depth gradient, disruptive selection is weak, the species are sexually monochromatic, yet assortative mating is strong. We infer that Lake Ejagham was colonized by Coptodon cichlids almost as soon as it came into existence 9,000 years ago, yet speciation events occurred only in the last 1,000-2,000 years. We show that secondary gene flow from a nearby riverine species has been ongoing, into ancestral as well as extant Lake Ejagham lineages, and we identify and date river-to-lake admixture blocks. One of these contains a cluster of olfactory receptor genes that introgressed close to the time of the first speciation event and coincides with a higher overall rate of admixture into the recipient lineages. Olfactory signaling is a key component of mate choice and species recognition in cichlids. A functional role for this introgression event is consistent with previous findings that assortative mating appears much stronger than ecological divergence in Ejagham Coptodon. We conclude that speciation in this radiation took place in sympatry, yet may have benefited from ongoing riverine gene flow.\n\nAuthor SummaryDespite an active search for empirical examples and much theoretical work, sympatric speciation remains one of the most controversial ideas in evolutionary biology. While a host of examples have been described in the last few decades, more recent results have shown that several of the most convincing systems have not evolved in complete isolation from allopatric populations after all. By itself, documenting the occurrence of secondary gene flow is not sufficient to reject the hypothesis of sympatric speciation, since speciation can still be considered sympatric if gene flow did not contribute significantly to the build-up of reproductive isolation. One way forward is to use genomic data to infer where, when and into which lineages gene flow occurred, and identify the regions of the genome that experienced admixture. In this study, we use whole-genome sequencing to examine one of the cichlid radiations from a small isolated Cameroon lake, which have long been the flagship example of sympatric speciation. We show that gene flow from a riverine species into the lake has been ongoing during the history of the radiation. In line with this, we infer that the lake was colonized very soon after it was formed, and argue that Lake Ejagham is not as isolated as previously assumed. The magnitude of secondary gene flow was relatively even across Lake Ejagham lineages, yet with some evidence for differential admixture, most notably before the first speciation event into the C. deckerti and C. ejagham lineage. Among the sequences that were introgressed into this lineage is a cluster of olfactory receptor genes, which may have facilitated speciation by promoting sexual isolation between incipient species, consistent with previous findings that sexual isolation appears to be stronger than ecological isolation in Ejagham Coptodon. We conclude that speciation in this radiation took place in sympatry, yet may have benefited from ongoing riverine gene flow.

evolutionary biology↗
bioRxiv2026

House fly proto-Y chromosomes differentially affect courtship success regardless of social context and female type

Genetic variation exists for many male reproductive traits despite apparent strong sexual selection in favor of particular males. Understanding how that variation is maintained is an unresolved problem in evolutionary biology. One proposed solution to this problem is genotype-by-environment interactions (GEIs), where no male genotype is universally superior across environments. Another proposed answer is variation in female preference, such that different females prefer different male genotypes. Additionally, male genotypes may differ in their reproductive output as they age. The house fly Musca domestica is a well-suited system to evaluate these explanations for genetic variation in male reproductive traits because two male genotypes (YM and IIIM) differ in mating performance. Specifically, IIIM males outcompete YM males in mating assays because IIIM males have a shorter copulation latency. To determine the relative importance of GEIs, female variation, and male age on the maintenance of genetic variation in male reproductive behaviors, we performed non-competitive (one male to one female) and competitive (one IIIM male and one YM male to one female) mating assays while considering multiple ages and different female strains. IIIM males attempted more matings regardless of competition level, female genotype or age, but mated faster than YM males only with females of their own strain and only performed more matings in non-competitive trials. However, female strain did not improve the mating success of YM males. We also did not observe evidence for genotype-by-age interactions on male mating success. Importantly, we did not identify any conditions where YM males outcompeted IIIM males, and therefore there was no evidence for interactions or trade-offs that could explain the maintenance of genetic variation for male mating success. To explain the maintenance of IIIM and YM males, other factors such as additional social environments or varying temperature should be investigated, as the genotypes are found in natural environments with contrasting temperatures.

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↗
bioRxiv2025

Parallel and non-parallel features of adaptive radiation in Yucatan pupfishes

Understanding the extent of parallelism across adaptive radiations remains a central problem in evolutionary biology. We used whole-genome resequencing of 123 individuals to compare the adaptive radiation of Cyprinodon pupfishes in Lake Chichancanab, Mexico, to an independent radiation of San Salvador Island (SSI) pupfishes in the Bahamas, and assess the repeatability of adaptive genetic architecture, sources of adaptive variation, and stages of selection. Despite rapid craniofacial divergence of trophic specialists within 8-15 kya, only two candidate genes (0.5%; 2/426) were shared between Caribbean radiations. Although adaptive introgression played a major role in SSI, we found minimal evidence of adaptive introgression in Chichancanab, likely due to the geographic isolation of this inland lake. Instead, de novo mutations provided a substantial source of adaptive variation (30.6%) for the endemic zooplanktivore, 15 times higher than the endemic scale-eater on SSI. However, in parallel with SSI, we found strong evidence that adaptive divergence occurred in stages, first on regulatory and standing genetic variation, then on de novo and nonsynonymous mutations. Consistent with adaptive variants near opsin and spermatogenesis genes, functional categories unique to Chichancanab, we found greater visual acuity and divergent sperm morphology in lab-reared zooplanktivores relative to generalists using laboratory assays. Consistent with extensive adaptive de novo mutations in WNT10A and rapid diversification of tooth size in the zooplanktivore, we found that experimental inhibition of the Wnt pathway in generalists resulted in narrower oral teeth. We conclude that de novo mutations, not introgression, can drive rapid adaptive radiations in isolated environments.

evolutionary biology↗
bioRxiv2020

Genomic signature of shifts in selection and alkaline adaptation in highland fish

Understanding how organisms adapt to aquatic life at high altitude is fundamental in evolutionary biology. This objective has been addressed primarily related to hypoxia adaptation by recent comparative studies, whereas highland fish has also long suffered extreme alkaline environment, insight into the genomic basis of alkaline adaptation has rarely been provided. Here, we compared the genomes or transcriptomes of 15 fish species, including two alkaline tolerant highland fish species and their six alkaline intolerant relatives, three alkaline tolerant lowland fish species and four alkaline intolerant species. We found putatively consistent patterns of molecular evolution in alkaline tolerant species in a large number of shared orthologs within highland and lowland fish taxa. Remarkably, we identified consistent signatures of accelerated evolution and positive selection in a set of shared genes associated with ion transport, apoptosis, immune response and energy metabolisms in alkaline tolerant species within both highland and lowland fish taxa. This is one of the first comparative studies that began to elucidate the consistent genomic signature of alkaline adaptation shared by highland and lowland fish. This finding also highlights the adaptive molecular evolution changes that support fish adapting to extreme environments at high altitude. Significance StatementLittle is known about how wild fish responds to extreme alkaline stress besides hypoxia at high altitude. Comparative genomics has begun to elucidate the genomic basis of alkaline adaptation in lowland fish, such as killifish, but insight from highland fish has lagged behind. The common role of adaptive molecular evolution during alkaline adaptation in highland and lowland fish has rarely been discussed. We address this question by comparing 15 fish omics data. We find numbers of shared orthologs exhibited consistent patterns of molecular evolution in alkaline tolerant species relative to intolerant species. We further identify remarkably consistent signatures of rapidly evolving and positive selection in a substantial shared core of genes in both highland and lowland alkaline tolerant species.

evolutionary biology↗
bioRxiv2023

Broad-scale signatures of linked selection under divergent recombination landscapes and mating systems in natural populations of rye and barley

Understanding the interactions between patterns of recombination, mating systems, and signatures of natural selection is a central aim in evolutionary biology. Patterns of recombination shape the evolution of genomes by affecting the efficacy of selection. Within populations, genetic shuffling is achieved through meiotic recombination, random chromosome segregation, and the frequency of outbreeding. Recombination landscapes vary between species and populations, and are further influenced by mating systems. Here, we use populations of two related grass species, rye (Secale cereale) and barley (Hordeum vulgare ssp. spontaneum), that differ in their mating system, to analyse signatures of linked selection under divergent recombination landscapes. Rye (outbreeding) and barley (inbreeding) are members of the Poaceae and diverged approximately 15 M years ago. We estimated population recombination rates, analysed patterns of genetic diversity, identified signatures of linked selection, and quantified the fraction and functional class of genes affected by linked selection. In this comparison, we detected signatures of linked selection in low-recombining regions in both species. In inbreeding barley, the low-recombining fraction of the genome was more than 2-fold larger than in outbreeding rye. Furthermore, considering differences in gene density across the genome, approximately 1.5 times more genes were affected by linked selection in barley than in rye. In both species, genomic regions affected by linked selection harbour mostly genes involved in basic cellular processes. We provide empirical evidence for quantitative differences in recombination landscapes between closely related species of divergent mating systems, and discuss the consequences of linked selection and the efficacy of natural selection. Significance statementThe ability of natural selection to disentangle beneficial from deleterious mutations across the genome is shaped by patterns of recombination, yet our understanding of the magnitude of this interaction is incomplete. In our work, we show that patterns of recombination differ between related outbreeding and inbreeding grass species, and that the efficacy of selection differs between them. We provide empirical evidence for quantitative differences in recombination landscapes and patterns of selection.

evolutionary biology↗