Adaptive Genetic Variation Research Articles

Rapid climate-driven evolution of the invasive species Mytilus galloprovincialis over the past century

Climate-driven adaptive genetic variation is one of the most important ways for organisms to tolerate environmental change and succeed in altered environments. To understand rapid climate-driven evolution, and how this evolution might shift biogeographic distributions in response to global change, we measured the adaptive genetic variation to the local environment of a marine invasive species Mytilus galloprovincialis. The genetic structure of eight populations from the Mediterranean Sea, northeastern Atlantic, northeastern Pacific, and northwestern Pacific were determined using genome-wide screens for single nucleotide polymorphisms. The relationships of genetic variation to environmental (seawater and air) temperature were analyzed using redundancy analysis and BayeScEnv analysis to evaluate the impacts of temperature on the genetic divergences among these eight populations. We found that the genetic compositions were significantly different among populations and the adaptive genetic variation was associated with temperature variables. Further, we identified some genetic markers exhibiting signatures of divergent selection in association with environmental features that can be used in the future to closely monitor adaptive variation in this species. Our results suggest that divergent climatic factors have driven adaptive genetic variation in M. galloprovincialis over the past century. The rapid evolutionary adaptation has played a pivotal role in enabling this species to invade a wide range of thermal habitats successfully. Species like M. galloprovincialis that possess high levels of genetic variation may not only be especially capable of invading new habitats with different environmental conditions, but also poised to cope rapidly and successfully with rising global temperatures.

Detection of Adaptive Genetic Diversity in Wild Potato Populations and Its Implications in Conservation of Potato Germplasm

A better understanding on how genetic diversity is structured at natural habitats can be helpful for exploration and acquisition of plant germplasm. Historically, studies have relied on DNA markers to elucidate potato genetic diversity. Current advances in genomics are broadening applications allowing the identification of markers linked to genomic regions under selection. Those markers, known as adaptive markers, unlock additional ways to value and organize germplasm diversity. For example, conservation priorities could be given to germplasm units containing markers associated to unique geographic identity, and/or linked to traits of tolerance to abiotic stresses. This study investigated if adaptive marker loci were possible to be identified in a large AFLP marker dataset of ninety-four populations of the wild potato species S. fendleri. These populations originated from six different mountain ranges in southern Arizona, USA. A total of 2094 polymorphic AFLP markers were used to conduct genetic diversity analyses of populations and mountain ranges. Adaptive markers were detected using Bayesian methods which distinguished marker loci departing significantly from frequencies expected under neutral models of genetic differentiation. This identified 16 AFLP loci that were considered to be adaptive. To contrast diversity parameters generated with each set of markers, analyses that included all the 2094 AFLP markers, and only the 16 adaptive markers were conducted. The results showed that both were efficient for establishing genetic associations among populations and mountain ranges. However, adaptive markers were better on revealing geographic patterns and identity which would suggest these markers were linked to selection at the natural sites. An additional test to determine if adaptive markers associated to climate variables found two loci associated to specific climate variables in populations from different regions but sharing similar environmental structure. The distribution of adaptive markers among populations revealed that only two were needed to build a core subset able to keep all the markers. This preliminary assessment shows that adaptive genetic diversity could offer an additional way to measure diversity in potato germplasm and to set up options for conservation and research.

Among-family variation in survival and gene expression uncovers adaptive genetic variation in a threatened fish.

Variation in among-family transcriptional responses to different environmental conditions can help to identify adaptive genetic variation, even prior to a selective event. Coupling differential gene expression with formal survival analyses allows for the disentanglement of treatment effects, required for understanding how individuals plastically respond to environmental stressors, from the adaptive genetic variation responsible for differential survival. We combined these two approaches to investigate responses to an emerging conservation issue, thiamine (vitamin B1 ) deficiency, in a threatened population of Atlantic salmon (Salmo salar). Thiamine is an essential vitamin that is increasingly limited in many ecosystems. In Lake Champlain, Atlantic salmon cannot acquire thiamine in sufficient quantities to support natural reproduction; fertilized eggs must be reared in hatcheries and treated with supplemental thiamine. We evaluated transcriptional responses (via RNAsequencing) to thiamine treatment across families and found 3,616 genes differentially expressed between control (no supplemental thiamine) and treatment individuals. Fewer genes changed expression equally across families (i.e., additively) than exhibited genotype×environment interactions in response to thiamine. Differentially expressed genes were related to known physiological effects of thiamine deficiency, including oxidative stress, cardiovascular irregularities and neurological abnormalities. We also identified 1,446 putatively adaptive genes that were strongly associated with among-family survival in the absence of thiamine treatment, many of which related to neurogenesis and visual perception. Our results highlight the utility of coupling RNA sequencing with formal survival analyses to identify candidate genes that underlie the among-family variation in survival required for an adaptive response to natural selection.

Into the bloom: Molecular response of pelagic tunicates to fluctuating food availability.

The planktonic tunicates appendicularians and thaliaceans are highly efficient filter feeders on a wide range of prey size including bacteria and have shorter generation times than any other marine grazers. These traits allow some tunicate species to reach high population densities and ensure their success in a favourable environment. However, there are still few studies focusing on which genes and gene pathways are associated with responses of pelagic tunicates to environmental variability. Herein, we present the effect of food availability increase on tunicate community and gene expression at the Marquesas Islands (South-East Pacific Ocean). By using data from the Tara Oceans expedition, we show that changes in phytoplankton density and composition trigger the success of a dominant larvacean species (an undescribed appendicularian). Transcriptional signature to the autotroph bloom suggests key functions in specific physiological processes, i.e., energy metabolism, muscle contraction, membrane trafficking, and proteostasis. The relative abundance of reverse transcription-related Pfams was lower at bloom conditions, suggesting a link with adaptive genetic diversity in tunicates in natural ecosystems. Downstream of the bloom, pelagic tunicates were outcompeted by copepods. Our work represents the first metaomics study of the biological effects of phytoplankton bloom on a key zooplankton taxon.

Genomic assessment of local adaptation in dwarf birch to inform assisted gene flow.

When populations of a rare species are small, isolated and declining under climate change, some populations may become locally maladapted. Detecting this maladaptation may allow effective rapid conservation interventions, even if based on incomplete knowledge. Population maladaptation may be estimated by finding genome–environment associations (GEA) between allele frequencies and environmental variables across a local species range, and identifying populations whose allele frequencies do not fit with these trends. We can then design assisted gene flow strategies for maladapted populations, to adjust their allele frequencies, entailing lower levels of intervention than with undirected conservation action. Here, we investigate this strategy in Scottish populations of the montane plant dwarf birch (Betula nana). In genome‐wide restriction site‐associated single nucleotide polymorphism (SNP) data, we found 267 significant associations between SNP loci and environmental variables. We ranked populations by maladaptation estimated using allele frequency deviation from the general trends at these loci; this gave a different prioritization for conservation action than the Shapely Index, which seeks to preserve rare neutral variation. Populations estimated to be maladapted in their allele frequencies at loci associated with annual mean temperature were found to have reduced catkin production. Using an environmental niche modelling (ENM) approach, we found annual mean temperature (35%), and mean diurnal range (15%), to be important predictors of the dwarf birch distribution. Intriguingly, there was a significant correlation between the number of loci associated with each environmental variable in the GEA and the importance of that variable in the ENM. Together, these results suggest that the same environmental variables determine both adaptive genetic variation and species range in Scottish dwarf birch. We suggest an assisted gene flow strategy that aims to maximize the local adaptation of dwarf birch populations under climate change by matching allele frequencies to current and future environments.

Landscape genomics predicts climate change-related genetic offset for the widespread Platycladus orientalis (Cupressaceae).

Understanding and quantifying populations' adaptive genetic variation and their response to climate change are critical to reforestation's seed source selection, forest management decisions, and gene conservation. Landscape genomics combined with geographic and environmental information provide an opportunity to interrogate forest populations' genome‐wide variation for understanding the extent to which evolutionary forces shape past and contemporary populations' genetic structure, and identify those populations that may be most at risk under future climate change. Here, we used genotyping by sequencing to generate over 11,000 high‐quality variants from Platycladus orientalis range‐wide collection to evaluate its diversity and to predict genetic offset under future climate scenarios. Platycladus orientalis is a widespread conifer in China with significant ecological, timber, and medicinal values. We found population structure and evidences of isolation by environment, indicative of adaptation to local conditions. Gradient forest modeling identified temperature‐related variables as the most important environmental factors influencing genetic variation and predicted areas with higher risk under future climate change. This study provides an important reference for forest resource management and conservation for P. orientalis.

An Aptitude for Altitude: Are Epigenomic Processes Involved?

In recent years, high-throughput genomic technologies and computational advancements have invigorated efforts to identify the molecular mechanisms regulating human adaptation to high altitude. Although exceptional progress regarding the identification of genomic regions showing evidence of recent positive selection has been made, many of the key “hypoxia tolerant” phenotypes of highland populations have not yet been linked to putative adaptive genetic variants. As a result, fundamental questions regarding the biological processes by which such adaptations are acquired remain unanswered. This Mini Review discusses the hypothesis that the epigenome works in coordination with underlying genomic sequence to govern adaptation to the chronic hypoxia of high altitude by influencing adaptive capacity and phenotypic variation under conditions of environmental hypoxia. Efforts to unravel the complex interactions between the genome, epigenome, and environmental exposures are essential to more fully appreciate the mechanisms underlying human adaptation to hypoxia.

Predicting Adaptive Genetic Variation of Loblolly Pine (Pinus taeda L.) Populations Under Projected Future Climates Based on Multivariate Models.

Greenhouse gas emission and global warming are likely to cause rapid climate change within the natural range of loblolly pine over the next few decades, thus bringing uncertainty to their adaptation to the environment. Here, we studied adaptive genetic variation of loblolly pine and correlated genetic variation with bioclimatic variables using multivariate modeling methods-Redundancy Analysis, Generalized Dissimilarity Modeling, and Gradient Forests. Studied trees (N = 299) were originally sampled from their native range across eight states on the east side of the Mississippi River. Genetic variation was calculated using a total of 44,317 single-nucleotide polymorphisms acquired by exome target sequencing. The fitted models were used to predict the adaptive genetic variation on a large spatial and temporal scale. We observed east-to-west spatial genetic variation across the range, which presented evidence of isolation by distance. Different key factors drive adaptation of loblolly pine from different geographical regions. Trees residing near the northeastern edge of the range, spanning across Delaware and Maryland and mountainous areas of Virginia, North Carolina, South Carolina, and northern Georgia, were identified to be most likely impacted by climate change based on the large difference in genetic composition under current and future climate conditions. This study provides new perspectives on adaptive genetic variation of loblolly pine in response to different climate scenarios, and the results can be used to target particular populations while developing adaptive forest management guidelines.

Pesticide contamination drives adaptive genetic variation in the endemic mayfly Andesiops torrens within a semi-arid agricultural watershed of Chile

Agrichemical contamination can provoke evolutionary responses in freshwater populations. It is a particularly relevant issue in semi-arid regions due to the sensitivity of endemic species to pollutants and to interactions with temperature stress. This paper investigates the presence of pesticides in rivers within a semi-arid agricultural watershed of Chile, testing for their effects on population genetic characteristics of the endemic mayfly Andesiops torrens (Insecta, Ephemeroptera). Pesticides were detected in sediment samples in ten out of the 30 sites analyzed throughout the upper part of the Limarí watershed. To study the evolutionary impact of such contamination on A. torrens, we used a genome-wide approach and analyzed 2056 single nucleotide polymorphisms (SNPs) loci in 551 individuals from all sites. Genetic differentiation was weak between populations, suggesting high gene flow across the study area. While we did not find evidence of pesticide effects on genetic diversity nor on population differentiation, the allele frequency of three outlier SNP loci correlated significantly with pesticide occurrence. Interrogation of genomic resources indicates that two of these SNPs are located within functional genes that encode for the low-density lipoprotein receptor-related protein 2 and Dumpy, both potentially involved in insect cuticle resistance processes. Such genomic signatures of local adaptation are indicative of past adverse effects of pesticide exposure on the locally adapted populations. Our results reveal that A. torrens is sensitive to pesticide exposure, but that a high gene flow may confer resilience to contamination. This research supports the contention that A. torrens is an ideal model organism to study evolutionary responses induced by pesticides on non-target, endemic species.

Novel signals of adaptive genetic variation in northwestern Atlantic cod revealed by whole-genome sequencing.

Selection can create complex patterns of adaptive differentiation among populations in the wild that may be relevant to management. Atlantic cod in the Northwest Atlantic are at a fraction of their historical abundance and a lack of recovery within the Gulf of Maine has created concern regarding the misalignment of fisheries management structures with biological population structure. To address this and investigate genome‐wide patterns of variation, we used low‐coverage sequencing to perform a region‐wide, whole‐genome analysis of fine‐scale population structure. We sequenced 306 individuals from 20 sampling locations in U.S. and Canadian waters, including the major spawning aggregations in the Gulf of Maine in addition to spawning aggregations from Georges Bank, southern New England, the eastern Scotian Shelf, and St. Pierre Bank. With genotype likelihoods estimated at almost 11 million loci, we found large differences in haplotype frequencies of previously described chromosomal inversions between Canadian and U.S. sampling locations and also among U.S. sampling locations. Our whole‐genome resolution also revealed novel outlier peaks, some of which showed significant genetic differentiation among sampling locations. Comparisons between allochronic winter‐ and spring‐spawning populations revealed highly elevated relative (FST) and absolute (dxy) genetic differentiation near genes involved in reproduction, particularly genes associated with the brain‐pituitary‐gonadal axis, which likely control timing of spawning, contributing to prezygotic isolation. We also found genetic differentiation associated with heat shock proteins and other genes of functional relevance, with complex patterns that may point to multifaceted selection pressures and local adaptation among spawning populations. We provide a high‐resolution picture of U.S. Atlantic cod population structure, revealing greater complexity than is currently recognized in management. Our genome‐scan approach likely underestimates the full suite of adaptive differentiation among sampling locations. Nevertheless, it should inform the revision of stock boundaries to preserve adaptive genetic diversity and evolutionary potential of cod populations.

Divergent selection and genetic structure of Sideritis scardica populations from southern Balkan Peninsula as revealed by AFLP fingerprinting

Sideritis scardica Giseb. is a subalpine/alpine plant species endemic to the central part of the Balkan Peninsula. In this study, we combined Amplified Fragment Length Polymorphism (AFLP) and environmental data to examine the adaptive genetic variations in S. scardica natural populations sampled in contrasting environments. A total of 226 AFLP loci were genotyped in 166 individuals from nine populations. The results demonstrated low gene diversity, ranging from 0.095 to 0.133 and significant genetic differentiation ranging from 0.115 to 0.408. Seven genetic clusters were revealed by Bayesian clustering methods as well as by Discriminant Analysis of Principal Components and each population formed its respective cluster. The exception were populations P02 Mt. Shara and P07 Mt. Vermio, that were admixed between two clusters. Both landscape genetic methods Mcheza and BayeScan identified a total of seven (3.10%) markers exhibiting higher levels of genetic differentiation among populations. The spatial analysis method Samβada detected 50 individual markers (22.12%) associated with bioclimatic variables, among them seven were identified by both Mcheza and BayeScan as being under directional selection. Four bioclimatic variables associated with five out of seven outliers were related to precipitation, suggesting that this variable is the key factor affecting the adaptive variation of S. scardica.

Testing the Effect of Mountain Ranges as a Physical Barrier to Current Gene Flow and Environmentally Dependent Adaptive Divergence in Cunninghamia konishii (Cupressaceae).

Populations can be genetically isolated by differences in their ecology or environment that hampered efficient migration, or they may be isolated solely by geographic distance. Moreover, mountain ranges across a species’ distribution area might have acted as barriers to gene flow. Genetic variation was quantified using amplified fragment length polymorphism (AFLP) and 13 selective amplification primer combinations used generated a total of 482 fragments. Here, we tested the barrier effects of mountains on gene flow and environmentally dependent local adaptation of Cunninghamia konishii occur in Taiwan. A pattern of genetic isolation by distance was not found and variation partitioning revealed that environment explained a relatively larger proportion of genetic variation than geography. The effect of mountains as barriers to genetic exchange, despite low population differentiation indicating a high rate of gene flow, was found within the distribution range of C. konishii. Twelve AFLP loci were identified as potential selective outliers using genome-scan methods (BAYESCAN and DFDIST) and strongly associated with environmental variables using regression approaches (LFMM, Samβada, and rstanarm) demonstrating adaptive divergence underlying local adaptation. Annual mean temperature, annual precipitation, and slope could be the most important environmental factors causally associated with adaptive genetic variation in C. konishii. The study revealed the existence of physical barriers to current gene flow and environmentally dependent adaptive divergence, and a significant proportion of the rate of gene flow may represent a reflection of demographic history.

Prioritizing natural-selection signals from the deep-sequencing genomic data suggests multi-variant adaptation in Tibetan highlanders.

Human genetic adaptation to high altitudes (>2500 m) has been extensively studied over the last few years, but few functional adaptive genetic variants have been identified, largely owing to the lack of deep-genome sequencing data available to previous studies. Here, we build a list of putative adaptive variants, including 63 missense, 7 loss-of-function, 1,298 evolutionarily conserved variants and 509 expression quantitative traits loci. Notably, the top signal of selection is located in TMEM247, a transmembrane protein-coding gene. The Tibetan version of TMEM247 harbors one high-frequency (76.3%) missense variant, rs116983452 (c.248C > T; p.Ala83Val), with the T allele derived from archaic ancestry and carried by >94% of Tibetans but absent or in low frequencies (<3%) in non-Tibetan populations. The rs116983452-T is strongly and positively correlated with altitude and significantly associated with reduced hemoglobin concentration (p = 5.78 × 10−5), red blood cell count (p = 5.72 × 10−7) and hematocrit (p = 2.57 × 10−6). In particular, TMEM247-rs116983452 shows greater effect size and better predicts the phenotypic outcome than any EPAS1 variants in association with adaptive traits in Tibetans. Modeling the interaction between TMEM247-rs116983452 and EPAS1 variants indicates weak but statistically significant epistatic effects. Our results support that multiple variants may jointly deliver the fitness of the Tibetans on the plateau, where a complex model is needed to elucidate the adaptive evolution mechanism.

Landscape genetics reveals that adaptive genetic divergence in Pinus bungeana (Pinaceae) is driven by environmental variables relating to ecological habitats

BackgroundUnderstanding the genetic basis of local adaptation has long been the concern of biologists. Identifying these adaptive genetic variabilities is crucial not only to improve our knowledge of the genetic mechanism of local adaptation but also to explore the adaptation potential of species.ResultsUsing 10 natural populations and 12 start codon targeted (SCoT) markers, a total of 430 unambiguous loci were yielded. The Bayesian analysis of population structure clearly demonstrated that the 10 populations of P. bungeana could be subdivided into three groups. Redundancy analysis showed that this genetic divergence was caused by divergence selection from environmental variables related to the ecological habitats of “avoidance of flooding” and “avoidance of high temperature and humidity.” LFMM results indicated that Bio1, Bio5, Bio8, Bio12, Bio14, and Bio16, which are related to the ecological habitat of P. bungeana, were correlated with the highest numbers of environment-associated loci (EAL).ConclusionsThe results of EAL characterization in P. bungeana clearly supported the hypothesis that environmental variations related to the ecological habitat of species are the key drivers of species adaptive divergence. Moreover, a method to calculate the species landscape adaptation index and quantify the adaptation potential of species was proposed and verified using ecological niche modeling. This model could estimate climatically suitable areas of species spatial distribution. Taking the results together, this study improves the current understanding on the genetic basis of local adaptation.

Adaptive Changes in Hemoglobin Function in High-Altitude Tibetan Canids Were Derived via Gene Conversion and Introgression.

A key question in evolutionary biology concerns the relative importance of different sources of adaptive genetic variation, such as de novo mutations, standing variation, and introgressive hybridization. A corollary question concerns how allelic variants derived from these different sources may influence the molecular basis of phenotypic adaptation. Here, we use a protein-engineering approach to examine the phenotypic effect of putatively adaptive hemoglobin (Hb) mutations in the high-altitude Tibetan wolf that were selectively introgressed into the Tibetan mastiff, a high-altitude dog breed that is renowned for its hypoxia tolerance. Experiments revealed that the introgressed coding variants confer an increased Hb–O2 affinity in conjunction with an enhanced Bohr effect. We also document that affinity-enhancing mutations in the β-globin gene of Tibetan wolf were originally derived via interparalog gene conversion from a tandemly linked β-globin pseudogene. Thus, affinity-enhancing mutations were introduced into the β-globin gene of Tibetan wolf via one form of intragenomic lateral transfer (ectopic gene conversion) and were subsequently introduced into the Tibetan mastiff genome via a second form of lateral transfer (introgression). Site-directed mutagenesis experiments revealed that the increased Hb–O2 affinity requires a specific two-site combination of amino acid replacements, suggesting that the molecular underpinnings of Hb adaptation in Tibetan mastiff (involving mutations that arose in a nonexpressed gene and which originally fixed in Tibetan wolf) may be qualitatively distinct from functionally similar changes in protein function that could have evolved via sequential fixation of de novo mutations during the breed’s relatively short duration of residency at high altitude.

The role of dispersal, selection, and timing of sampling on the false discovery rate of loci under selection during geographic range expansion.

Identifying adaptive loci is important to understand the evolutionary potential of species undergoing range expansion. However, in expanding populations, spatial demographic processes such as allele surfing can create spatial patterns of neutral genetic variation that appear similar to those generated through adaptive processes. As a result, the false discovery rate of adaptive loci may be inflated in landscape genomic analyses. Here, we take a simulation modelling approach to investigate how range expansion affects our ability to correctly distinguish between neutral and adaptive genetic variation, using the mountain pine beetle outbreak system as a motivating example. We simulated the demographic and population genetic dynamics of populations undergoing range expansion using an individual-based genetic model CDMetaPOP. We investigated how the false discovery rate of adaptive loci is affected by (i) dispersal capacity, (ii) timing of sampling, and (iii) the strength of selection on an adaptive reference locus. We found that a combination of weak dispersal, weak selection, and early sampling presents the greatest risk of misidentifying loci under selection. Expanding populations present unique challenges to the reliable identification of adaptive loci. We demonstrate that there is a need for further methodological development to account for directional demographic processes in landscape genomics.

Cold adaptation in the Asian tiger mosquito's native range precedes its invasion success in temperate regions.

Adaptation to environmental conditions within the native range of exotic species can condition the invasion success of these species outside their range. The striking success of the Asian tiger mosquito, Aedes albopictus, to invade temperate regions has been attributed to the winter survival of diapause eggs in cold environments. In this study, we evaluate genetic polymorphisms (SNPs) and wing morphometric variation among three biogeographical regions of the native range of A. albopictus. Reconstructed demographic histories of populations show an initial expansion in Southeast Asia and suggest that marine regression during late Pleistocene and climate warming after the last glacial period favored expansion of populations in southern and northern regions, respectively. Searching for genomic signatures of selection, we identified significantly differentiated SNPs among which several are located in or within 20kb distance from candidate genes for cold adaptation. These genes involve cellular and metabolic processes and several of them have been shown to be differentially expressed under diapausing conditions. The three biogeographical regions also differ for wing size and shape, and wing size increases with latitude supporting Bergmann's rule. Adaptive genetic and morphometric variation observed along the climatic gradient of A. albopictus native range suggests that colonization of northern latitudes promoted adaptation to cold environments prior to its worldwide invasion.

Wave exposure as a driver of isolation by environment in the marine gastropod Nucella lapillus

The way adaptive and neutral genetic variation is shaped by environmental factors is crucial for evolutionary biology. To investigate whether wave exposure can enhance local adaptation on littoral snails, AFLP markers were scanned across ten populations of Nucella lapillus from contrasting habitats (protected vs. exposed). As some 6% of the analysed loci deviated from neutral expectations, it was suggested that wave exposure could be a strong selective agent shaping genetic variation. Neutral markers described a pattern of “Isolation by distance (IBD) only” with no signature of Isolation by environment (IBE), whereas loci under divergent selection followed a pattern of “IBD and IBE”, as Partial Mantel tests detected a significant IBD after accounting for environmental differences. The topology of genetic networks revealed a substantial gene flow at neutral markers (i.e. dense net with edges connecting similar and contrasting habitats), whereas few connections were established between contrasting environments at loci under divergent selection. Furthermore, loci correlated to phenotype (shell shape; i.e. a morphological biomarker of wave exposure) explained up to ca 11% of the variance of this trait. Altogether, our results suggest that, even in a context of gene flow, local adaptation could outline a feature such as shell shape.

Rare genetic variation and balanced polymorphisms are important for survival in global change conditions.

Standing genetic variation is important for population persistence in extreme environmental conditions. While some species may have the capacity to adapt to predicted average future global change conditions, the ability to survive extreme events is largely unknown. We used single-generation selection experiments on hundreds of thousands of Strongylocentrotus purpuratus sea urchin larvae generated from wild-caught adults to identify adaptive genetic variation responsive to moderate (pH 8.0) and extreme (pH 7.5) low-pH conditions. Sequencing genomic DNA from pools of larvae, we identified consistent changes in allele frequencies across replicate cultures for each pH condition and observed increased linkage disequilibrium around selected loci, revealing selection on recombined standing genetic variation. We found that loci responding uniquely to either selection regime were at low starting allele frequencies while variants that responded to both pH conditions (11.6% of selected variants) started at high frequencies. Loci under selection performed functions related to energetics, pH tolerance, cell growth and actin/cytoskeleton dynamics. These results highlight that persistence in future conditions will require two classes of genetic variation: common, pH-responsive variants maintained by balancing selection in a heterogeneous environment, and rare variants, particularly for extreme conditions, that must be maintained by large population sizes.

Local and regional scale habitat heterogeneity contribute to genetic adaptation in a commercially important marine mollusc (Haliotis rubra) from southeastern Australia.

Characterising adaptive genetic divergence among conspecific populations is often achieved by studying genetic variation across defined environmental gradients. In marine systems this is challenging due to a paucity of information on habitat heterogeneity at local and regional scales and a dependency on sampling regimes that are typically limited to broad longitudinal and latitudinal environmental gradients. As a result, the spatial scales at which selection processes operate and the environmental factors that contribute to genetic adaptation in marine systems are likely to be unclear. In this study we explore patterns of adaptive genetic structuring in a commercially- harvested abalone species (Haliotis rubra) from southeastern Australia, using a panel of genome-wide SNP markers (5,239 SNPs), and a sampling regime informed by marine LiDAR bathymetric imagery and 20-year hindcasted oceanographic models. Despite a lack of overall genetic structure across the sampling distribution, significant genotype associations with heterogeneous habitat features were observed at local and regional spatial scales, including associations with wave energy, ocean current, sea surface temperature, and geology. These findings provide insights into the potential resilience of the species to changing marine climates and the role of migration and selection on recruitment processes, with implications for conservation and fisheries management. This study points to the spatial scales at which selection processes operate in marine systems and highlights the benefits of geospatially-informed sampling regimes for overcoming limitations associated with marine population genomic research.