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Nunez, J. C. B.

Publications and source records attributed to Nunez, J. C. B..

15 recordsLinked to original sources

Revealing the abiotic and biotic drivers of past and future local adaptation in a coastal dogwhelk

Predicting whether populations can persist under rapid environmental change requires identifying the ecological drivers of local adaptation, uncovering their genetic bases, and understanding how adaptive variation will respond to future selection. Here, we combine landscape genomics, environmental data, and evolutionary simulations to identify the selective forces shaping adaptation across 1,500 km of the west coast of North America in the low-dispersing coastal dogwhelk Nucella canaliculata, determine their genomic bases, and forecast future evolutionary responses. We found strong associations of genome-wide variation with both abiotic (i.e., mean pH) and biotic variation (i.e., cross-sectional shell thickness of the mussel prey species, Mytilus californianus). These patterns are underlain by two large-effect loci, including a biomineralization gene associated with pH tolerance and a locus near a thiamine transporter associated with prey shell thickness. Genomic offset analyses and population genetic simulations further predict that ongoing ocean acidification will disrupt existing adaptive patterns and generate maladaptation in high latitude populations, with evolutionary outcomes strongly influenced by gene flow, which determines the rate at which adaptive alleles spread across the species range. Together, these findings reveal how biotic and abiotic selective pressures shape adaptive genomic variation and provide a framework for forecasting evolutionary responses to future global change.

evolutionary biology↗

A novel CTmax assay reveals divergent thermal acclimation capacity across three ecologically distinct sea urchins

Global change is driving rapid ocean warming, exposing organisms to both chronic temperature increases and acute marine heatwaves. Understanding how species cope with thermal stress is critical for predicting ecosystem resilience. Echinoderms are globally distributed and often function as foundational species, yet comparative assessments of upper thermal tolerance among species occupying contrasting thermal environments remain limited. Here, we address this gap by comparing upper thermal tolerance across three sea urchins with distinct biogeographic distributions: the latitudinally broad purple sea urchin (Strongylocentrotus purpuratus), the circumpolar green sea urchin (S. droebachiensis), and the tropical variegated sea urchin (Lytechinus variegatus). We quantified thermal limits after two acclimation treatments: ambient temperatures approximating native habitat conditions for each species and an elevated temperature (+6 C). We developed a novel assay to measure critical thermal maximum (CTmax), comparing variability and inconsistencies associated among multiple assays. Upper thermal tolerance increased with acclimation to elevated temperatures in all three species, but acclimatory capacity differed markedly, with S. droebachiensis showing the strongest response and S. purpuratus the weakest. Conversely, S. purpuratus had the highest thermal safety margin and thus the lowest proximity to its thermal ceiling. Our adhesion based CTmax method was more reproducible and the most precise compared to other metrics tested, providing an improved framework for quantifying physiological thermal limits of sea urchins. Together, these findings reveal substantial but unevenly distributed thermal resilience in ecologically diverse sea urchins, advancing our understanding of how foundational marine species may respond to future global change.

evolutionary biology↗

A general model for the evolution of thermal performance curves with application to real time-series data

Thermal performance curves (TPCs) are widely used to investigate the effect of changes in body temperature on an organisms performance. Despite empirical evidence that temperature-dependent performance is ubiquitous across taxa, the field lacks models for how thermal performance evolves under realistic timeseries, genetic architectures, and physiological constraints. We address this gap by integrating a mathematical model with individual-based quantitative population genetic simulations. Our model can predict the evolutionary trajectory and shape of TPCs for any given thermal regime. Our model reproduces core properties of TPC evolution from previous studies such as the emergence of generalists in variable environments, but also explains why organisms may evolve TPCs that do not match their historical body temperature range. We uncover novel dynamics of adaptive tracking, the most notable being multi-generation lags between temperature and TPC parameters that can lead to unexpected correlations between the two. Our model predicts empirically observed patterns of adaptive tracking of critical thermal minimum in the invasive pest Drosophila suzukii, including individual-level variability and multi-generation lags with changing temperature. Our results also highlight the limitations of models that ignore factors that influence TPC evolution and individual variability, such as autocorrelation in temperature timeseries, effective population size, evolution of additive genetic correlation in TPC parameters, genetic architecture, and physiological constraints. Our flexible simulation model can incorporate these factors and help generate empirically testable hypotheses of how species will evolve in response to global climate change.

evolutionary biology↗

Phenotypic and Genomic Evidence of Adaptive Tracking in Thermal Tolerance of Wild Populations of an Invasive Drosophila.

Adaptive tracking is an evolutionary process in which allele frequencies and phenotypes shift in response to temporally fluctuating environments. Currently it is unclear whether adaptive tracking causes predictable evolution of complex traits such as thermal tolerance. We investigated seasonal adaptive tracking of critical thermal minimum (CTmin) and genome-wide allele frequencies over multiple years in the invasive fly Drosophila suzukii. CTmin increased throughout the growing season, showing a lag of several generations between increasing temperature and evolutionary change. Genetic analyses indicate CTmin is highly polygenic, with little overlap between alleles associated with CTmin and other seasonally fluctuating alleles. Thus, polygenic traits may track seasonal environments without leaving strong genomic signals. By contrast, there were strong seasonal genomic signatures for alleles associated with oligogenic traits as such pesticide resistance and olfactory behavior. These findings suggest that seasonal adaptive tracking shapes a broad suite of traits that contribute to D. suzukiis invasion success.

evolutionary biology↗

Evidence of Adaptation in Structural Variants among Wild Populations of the purple sea urchin, Strongylocentrotus purpuratus

Structural variants (SVs) are increasingly recognized as important components of genetic architecture, complementing and extending beyond traditionally studied single nucleotide polymorphisms. Though growing, our understanding of the evolutionary forces maintaining SVs in natural populations is limited. Chromosomal inversions in particular can facilitate local adaptation in populations with high gene flow, including many marine species. The purple sea urchin (Strongylocentrotus purpuratus) is a powerful system to study these dynamics due to its high gene flow, lack of population structure, and broad latitudinal range. We analyzed whole genome sequence data from 137 individuals from seven populations to identify structural variants using local PCA, linkage disequilibrium, and FST analyses. We integrated Bayesian selection scans and population genetic statistics to test for signatures of selection in putative inversions. We identified nine loci showing signatures consistent with inversion polymorphisms, including three-way genotype clustering, long range linkage, and the characteristic hanging-bridge pattern. These loci are polymorphic within sites and along the species range with three loci showing concordant signatures of selection based on enrichment of XTX outliers and distinct patterns of allelic age consistent with positive and balancing selection. In addition, these loci show enrichment for genes associated with biomineralization and development. Our results are the first instance of identifying putative inversions in the purple sea urchin, adding to the genomic repertoire of this model species. Our results add to the growing evidence that chromosomal inversions are a key component of standing genetic variation in natural populations with an important role in adaptation to heterogeneous environments. Significance statementChromosomal inversion polymorphisms are an important part of the repertoire of standing genetic variation in wild populations and can facilitate adaptation in the face of strong gene flow. The purple sea urchin, a widely studied marine species, exhibits high gene flow, large population sizes, and extensive genetic diversity across diverse environmental conditions, making it an ideal model for evolutionary genomics. We identified nine putative inversions, three with signatures of selection, adding echinoderms to the growing list of phyla with putatively adaptive inversions. These findings provide new insights into structural variation in a highly dispersive marine species and highlight potential evolutionary mechanisms maintaining these polymorphisms.

evolutionary biology↗

Geographic Divergence in Population Genomics and Shell Morphology Reveal History of Glacial Refugia in a Coastal Dogwhelk

Studying contemporaneous spatial patterns of genomic diversity can yield important insights into the evolutionary processes that structure populations and shape patterns of adaptation. In contrast to the large number of marine species with planktonic larvae, populations of marine taxa with low dispersal and deep evolutionary divergences offer an opportunity to reveal the phylogeographic histories of marine ecosystems. Here, we constructed a draft genome assembly for the low-dispersing marine dogwhelk, Nucella canaliculata, and studied patterns of genomic diversity and shell morphometrics in 19 populations distributed along [~]1,500 km of the west coast of North America. We observed significant population structure with a strong phylogeographic break at Monterey Bay, which was matched with divergence in shell morphology. Genomic patterns, concomitant with computer simulations, suggest that there were at least two refugial populations during the last glacial maximum that subsequently experienced post-glacial expansion and admixture. Lastly, linking genotype to phenotype, we identified candidate loci underlying variation in shell morphology. These findings demonstrate how high-resolution genomic data reveal the roles of demography, selection, and historical events in shaping the spatial distribution of genetic variation, offering key insights into the processes that structure modern coastal populations and their potential to respond to future climatic changes.

evolutionary biology↗

Early life-stage thermal resilience is determined by climate-linked regulatory variation

Despite decades of research in environmental change, we know relatively little about the genetics of environmentally influenced traits across the life cycle of species with complex life histories. Previously, we reported that natural variation in heat tolerance is life-stage specific in Drosophila melanogaster, suggesting that thermal selection predominantly targets the early embryonic life stage. Here, we used advanced introgression and pooled whole-genome resequencing to map the genomic basis of enhanced embryonic heat tolerance in a neotropical line of D. melanogaster. We identified two loci on chromosomes 2R and X that were consistently targeted by 16 generations of thermal selection across six replicate introgressions. We compared alleles in these regions to published datasets of natural variation from North America and Europe using the DEST dataset. This analysis revealed that two SNPs associated with embryonic heat tolerance exhibited both clinal and seasonal patterns, with the seasonal variation significantly correlated with environmental variability in average precipitation and temperature variance across space and time. Further, tropical alleles at both loci exhibited enhanced embryonic heat tolerance in the Drosophila Genetics Reference Panel (DGRP), demonstrating the genotype-to-phenotype link in an independent set of diverse genetic backgrounds. The two SNPs lie in the putative regulatory regions of the genes SP70 and sog, where allelic differences in gene expression correlate with the heat tolerance phenotype. Overall, our results suggest that regulatory loci that influence embryonic heat tolerance are under selection in nature. Our study extends previous work in developmental genetics of Drosophila by characterizing the genomics of an ecologically relevant developmental trait in natural populations. Significance StatementBy comparing populations from distinct environments, we can determine the factors important for responses to environmental change. We used laboratory-based selection and whole-genome sequencing to uncover the genomic basis of embryonic heat tolerance in tropical and temperate fruit flies. We compared our results to published genomes of wild-collected flies from multiple continents and seasons. Strikingly, variants of two genes that influence embryonic heat tolerance are correlated with precipitation and temperature in natural populations. Further, different genetic variants produce distinct patterns of gene expression in response to heat stress. This is strong evidence that embryonic heat tolerance is under selection in nature and should be considered when forming predictions about responses to environmental change in species with complex life cycles.

evolutionary biology↗

Microbiome composition shapes temperature tolerance in a Hawaiian picture-winged Drosophila

Hawaiian picture-winged Drosophila are undergoing rapid biodiversity loss, with twelve species listed as endangered and others in decline. Gut microbiota are increasingly recognized as contributors to host adaptation that are capable of influencing stress tolerance, reproduction, and other fitness-related traits. We investigated the role of microbial communities in local adaptation using two populations of Drosophila basisetae from Hawaiian rainforests at 900 m and 1200 m elevation. Microbiome profiling of wild flies by high throughput amplicon sequencing revealed distinct bacterial and fungal communities between sites. Whole-genome resequencing of the two Drosophila populations identified weak but significant population genetic structure, with evidence of admixture and gene flow. Despite this connectivity, 16 outlier SNPs across 18 genes showed patterns consistent with divergent selection, suggesting localized adaptation. To test microbiome effects on host physiology experimentally, we conducted a fully factorial research design with microbiome inoculations in laboratory-reared flies acclimated to 18 {degrees}C (control) or 24 {degrees}C (stressful). Flies treated with low-elevation microbiota had higher survival across temperatures, whereas those treated with high-elevation microbiota produced more eggs, indicating microbiome-mediated differences in reproductive investment. Activity levels at 18 {degrees}C were higher when flies received microbiota from their native population. Measures of critical thermal maximum (CTmax) and male accessory gland size showed complex interactions among microbiome source, temperature, and fly population. These results indicate that microbes may modulate host thermal tolerance and reproduction in environmentally-dependent and population-specific ways. Our findings suggest that microbiome-host-environment interactions may contribute to both phenotypic plasticity and evolutionary adaptation to enhance resilience to environmental stress, with important implications for conservation in rapidly changing Hawaiian ecosystems. Summary statementThis study demonstrates that microbiome composition influences thermal tolerance through alterations in survival and reproduction in the Hawaiian picture wing, Drosophila basisetae, potentially contributing to adaptive phenotypic changes between populations.

evolutionary biology↗

Footprints of worldwide adaptation in structured populations of D. melanogaster through the expanded DEST 2.0 genomic resource

Large scale genomic resources can place genetic variation into an ecologically informed context. To advance our understanding of the population genetics of the fruit fly Drosophila melanogaster, we present an expanded release of the community-generated population genomics resource Drosophila Evolution over Space and Time (DEST 2.0; https://dest.bio/). This release includes 530 high-quality pooled libraries from flies collected across six continents over more than a decade (2009-2021), most at multiple time points per year; 211 of these libraries are sequenced and shared here for the first time. We used this enhanced resource to elucidate several aspects of the species demographic history and identify novel signs of adaptation across spatial and temporal dimensions. We showed that patterns of secondary contact, originally characterized in North America, are replicated in South America and Australia. We also found that the spatial genetic structure of populations is stable over time, but that drift due to seasonal contractions of population size causes populations to diverge over time. We identified signals of adaptation that vary between continents in genomic regions associated with xenobiotic resistance, consistent with independent adaptation to common pesticides. Moreover, by analyzing samples collected during spring and fall across Europe, we provide new evidence for seasonal adaptation related to loci associated with pathogen response. Furthermore, we have also released an updated version of the DEST genome browser. This is a useful tool for studying spatio-temporal patterns of genetic variation in this classic model system.

evolutionary biology↗

Balancing selection and the functional effects of shared polymorphism in cryptic Daphnia species

The patterns of genetic variation within and between related taxa represent the genetic history of a species. Shared polymorphisms, loci with identical alleles across species, are of unique interest as they may represent cases of ancient selection maintaining functional variation post-speciation. In this study, we investigate the abundance of shared polymorphism in the Daphnia pulex species complex. We test whether shared mutations are consistent with the action of balancing selection or alternative hypotheses such as hybridization, incomplete lineage sorting, or convergent evolution. We analyzed over 2,000 genomes from North American and European D. pulex and several outgroup species to examine the prevalence and distribution of shared alleles between the focal species pair, North American and European D. pulex. We show that while North American and European D. pulex diverged over ten million years ago, they retained tens of thousands of shared alleles. We found that the number of shared polymorphisms between North American and European D. pulex cannot be explained by hybridization or incomplete lineage sorting alone. Instead, we show that most shared polymorphisms could be the product of convergent evolution, that a limited number appear to be old trans-specific polymorphisms, and that balancing selection is affecting young and ancient mutations alike. Finally, we provide evidence that a blue wavelength opsin gene with trans-specific polymorphisms has functional effects on behavior and fitness in the wild. Ultimately, our findings provide insights into the genetic basis of adaptation and the maintenance of genetic diversity between species.

evolutionary biology↗

A cosmopolitan inversion drives seasonal adaptation in overwintering Drosophila

Drosophila melanogaster living in temperate regions evolve as they track seasonal fluctuations. Yet, we lack an understanding of the genetic architecture of seasonal adaptive tracking. By sequencing orchard populations collected across multiple years, we characterized the genomic signal of seasonal demography and identified that the cosmopolitan inversion In(2L)t drives seasonal adaptation. In(2L)t shows footprints of selection that are inconsistent with simple explanations of genetic drift, as well as signatures of partial selective sweeps. A meta-analysis of phenotypic studies shows that seasonal loci within In(2L)t are associated with behavior, life-history, physiology, and morphology traits. Our results identify candidate regions that underlie seasonal adaptive tracking and link them to phenotype. This work supports the general hypothesis that inversions are important drivers of rapid adaptation. One-Sentence SummaryA chromosomal inversion drives adaptive evolution between seasons in wild fruit flies.

evolutionary biology↗

Polygenic variation in sexual investment across an ephemerality gradient in Daphnia pulex

Species across the tree of life can switch between asexual and sexual reproduction. In facultatively sexual species, the ability to switch between reproductive modes is often environmentally dependent and subject to local adaptation. However, the ecological and evolutionary factors that influence the maintenance and turnover of polymorphism associated with facultative sex remain unclear. To address this basic question, we studied the ecological and evolutionary dynamics of polymorphism in reproductive strategy in a metapopulation of the model facultative sexual, Daphnia pulex, located in the southern United Kingdom. We found that patterns of clonal diversity, but not genetic diversity varied with ephemerality. Reconstruction of a multi-year pedigree demonstrated the co-existence of clones that were found to differ in their investment into male production. Mapping of quantitative variation in male production using lab-generated and field-collected individuals identified multiple putative QTL underlying this trait, and we identified a plausible candidate gene. The evolutionary history of these QTL suggests that they are relatively young, and male limitation in this system is a rapidly evolving trait. Our work highlights the dynamic nature of the genetic structure and composition of facultative sex across space and time and suggests that quantitative genetic variation in reproductive strategy can undergo rapid evolutionary turnover.

evolutionary biology↗

Drosophila Evolution over Space and Time (DEST) - A New Population Genomics Resource

Drosophila melanogaster is a leading model in population genetics and genomics, and a growing number of whole-genome datasets from natural populations of this species have been published over the last 20 years. A major challenge is the integration of these disparate datasets, often generated using different sequencing technologies and bioinformatic pipelines, which hampers our ability to address questions about the evolution and population structure of this species. Here we address these issues by developing a bioinformatics pipeline that maps pooled sequencing (Pool-Seq) reads from D. melanogaster to a hologenome consisting of fly and symbiont genomes and estimates allele frequencies using either a heuristic (PoolSNP) or a probabilistic variant caller (SNAPE-pooled). We use this pipeline to generate the largest data repository of genomic data available for D. melanogaster to date, encompassing 271 population samples from over 100 locations in >20 countries on four continents based on a combination of 121 unpublished and 150 previously published genomic datasets. Several of these locations have been sampled at different seasons across multiple years. This dataset, which we call Drosophila Evolution over Space and Time (DEST), is coupled with sampling and environmental meta-data. A web-based genome browser and web portal provide easy access to the SNP dataset. Our aim is to provide this scalable platform as a community resource which can be easily extended via future efforts for an even more extensive cosmopolitan dataset. Our resource will enable population geneticists to analyze spatio-temporal genetic patterns and evolutionary dynamics of D. melanogaster populations in unprecedented detail.

genomics↗

Note: Updating the metadata of four misidentified samples in the DrosRTEC dataset

This note details the consortiums rationale behind its decision to modify the metadata for putatively misidentified European samples in the DrosRTEC dataset. In brief, we use PCA on published datasets from North America and Europe to generate phylogeographic clusters reflective of worldwide D. melanogaster demography. We used this PCA to train a DAPC model in order the predict the group membership. Our results indicate that 4 out of 73 samples were misclassified and the metadata was updated accordingly. These samples are a spring-fall pair from Spain and Austria.

genomics↗

Ecological load and balancing selection in circumboreal barnacles

Acorn barnacle adults experience environmental heterogeneity at various spatial scales of their circumboreal habitat, raising the question of how adaptation to high environmental variability is maintained in the face of strong juvenile dispersal and mortality. Here we show that 4% of genes in the barnacle genome experience balancing selection across the entire range of the species. Many of these genes harbor mutations maintained across 2 million years of evolution between the Pacific and Atlantic oceans. These genes are involved in ion regulation, pain reception, and heat tolerance, functions which are essential in highly variable ecosystems. The data also reveal complex population structure within and between basins, driven by the trans-Arctic interchange and the last glaciation. Divergence between Atlantic and Pacific populations is high, foreshadowing the onset of allopatric speciation, and suggesting that balancing selection is strong enough to maintain functional variation for millions of years in the face of complex demography.

evolutionary biology↗