Signatures Of Local Adaptation Research Articles

Local adaptation in populations of Mycobacterium tuberculosis endemic to the Indian Ocean Rim

Background: Lineage 1 (L1) and 3 (L3) are two lineages of the Mycobacterium tuberculosis complex (MTBC) causing tuberculosis (TB) in humans. L1 and L3 are prevalent around the rim of the Indian Ocean, the region that accounts for most of the world’s new TB cases. Despite their relevance for this region, L1 and L3 remain understudied. Methods: We analyzed 2,938 L1 and 2,030 L3 whole genome sequences originating from 69 countries. We reconstructed the evolutionary history of these two lineages and identified genes under positive selection. Results: We found a strongly asymmetric pattern of migration from South Asia toward neighboring regions, highlighting the historical role of South Asia in the dispersion of L1 and L3. Moreover, we found that several genes were under positive selection, including genes involved in virulence and resistance to antibiotics. For L1 we identified signatures of local adaptation at the esxH locus, a gene coding for a secreted effector that targets the human endosomal sorting complex, and is included in several vaccine candidates. Conclusions: Our study highlights the importance of genetic diversity in the MTBC, and sheds new light on two of the most important MTBC lineages affecting humans.

Local environment-driven adaptive evolution in a marine invasive ascidian (Molgula manhattensis).

Elucidating molecular mechanisms of environment‐driven adaptive evolution in marine invaders is crucial for understanding invasion success and further predicting their future invasions. Although increasing evidence suggests that adaptive evolution could contribute to organisms’ adaptation to varied environments, there remain knowledge gaps regarding how environments influence genomic variation in invaded habitats and genetic bases underlying local adaptation for most marine invaders. Here, we performed restriction‐site‐associated DNA sequencing (RADseq) to assess population genetic diversity and further investigate genomic signatures of local adaptation in the marine invasive ascidian, Molgula manhattensis. We revealed that most invasive populations exhibited significant genetic differentiation, low recent gene flow, and no signal of significant population bottleneck. Based on three genome scan approaches, we identified 109 candidate loci potentially under environmental selection. Redundancy analysis and variance partitioning analysis suggest that local environmental factors, particularly the salinity‐related variables, represent crucial evolutionary forces in driving adaptive divergence. Using the newly developed transcriptome as a reference, 14 functional genes were finally obtained with potential roles in salinity adaptation, including SLC5A1 and SLC9C1 genes from the solute carrier gene (SLC) superfamily. Our findings confirm that differed local environments could rapidly drive adaptive divergence among invasive populations and leave detectable genomic signatures in marine invaders.

Pervasive Genomic Signatures of Local Adaptation to Altitude Across Highland Specialist Andean Hummingbird Populations.

Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them "taller" biogeographic barriers.

Disentangling Ethiopian Honey Bee (Apis mellifera) Populations Based on Standard Morphometric and Genetic Analyses.

Simple SummaryWe conducted this population study of Ethiopian honey bees, using morphometric and genetic methods, to decipher their controversial classification. These honey bees are highly diverse and showed differentiation based on size and genetic information according to prevailing agro-ecological conditions, demonstrating morphological and molecular signatures of local adaptation. The results of both morphometric and genetic analyses suggest that Ethiopian honey bees differ from populations in the neighboring geographic regions and are characterized by extensive gene flow within the country, enhanced by honey bee colony trade. Consequently, future research that includes studying traits of vitality, behavior and colony performance of honey bees in remaining pocket areas of highland agro-ecological zones could contribute to the development of appropriate conservation management.The diversity and local differentiation of honey bees are subjects of broad general interest. In particular, the classification of Ethiopian honey bees has been a subject of debate for decades. Here, we conducted an integrated analysis based on classical morphometrics and a putative nuclear marker (denoted r7-frag) for elevational adaptation to classify and characterize these honey bees. Therefore, 660 worker bees were collected out of 66 colonies from highland, midland and lowland agro-ecological zones (AEZs) and were analyzed in reference to populations from neighboring countries. Multivariate morphometric analyses show that our Ethiopian samples are separate from Apis mellifera scutellata, A. m. jemenitica, A. m. litorea and A. m. monticola, but are closely related to A. m. simensis reference. Linear discriminant analysis showed differentiation according to AEZs in the form of highland, midland and lowland ecotypes. Moreover, size was positively correlated with elevation. Similarly, our Ethiopian samples were differentiated from A. m. monticola and A. m. scutellata based on r7-frag. There was a low tendency towards genetic differentiation between the Ethiopian samples, likely impacted by increased gene flow. However, the differentiation slightly increased with increasing elevational differences, demonstrated by the highland bees that showed higher differentiation from the lowland bees (FST = 0.024) compared to the midland bees (FST = 0.015). An allelic length polymorphism was detected (denoted as d) within r7-frag, showing a patterned distribution strongly associated with AEZ (X2 = 11.84, p < 0.01) and found predominantly in highland and midland bees of some pocket areas. In conclusion, the Ethiopian honey bees represented in this study are characterized by high gene flow that suppresses differentiation.

Local adaptation in populations of Mycobacterium tuberculosis endemic to the Indian Ocean Rim.

Background: Lineage 1 (L1) and 3 (L3) are two lineages of the Mycobacterium tuberculosis complex (MTBC) causing tuberculosis (TB) in humans. L1 and L3 are prevalent around the rim of the Indian Ocean, the region that accounts for most of the world's new TB cases. Despite their relevance for this region, L1 and L3 remain understudied. Methods: We analyzed 2,938 L1 and 2,030 L3 whole genome sequences originating from 69 countries. We reconstructed the evolutionary history of these two lineages and identified genes under positive selection. Results: We found a strongly asymmetric pattern of migration from South Asia toward neighboring regions, highlighting the historical role of South Asia in the dispersion of L1 and L3. Moreover, we found that several genes were under positive selection, including genes involved in virulence and resistance to antibiotics . For L1 we identified signatures of local adaptation at the esxH locus, a gene coding for a secreted effector that targets the human endosomal sorting complex, and is included in several vaccine candidates. Conclusions: Our study highlights the importance of genetic diversity in the MTBC, and sheds new light on two of the most important MTBC lineages affecting humans.

Little parallelism in genomic signatures of local adaptation in two sympatric, cryptic sister species.

Species living in sympatry and sharing a similar niche often express parallel phenotypes as a response to similar selection pressures. The degree of parallelism within underlying genomic levels is often unexplored, but can give insight into the mechanisms of natural selection and adaptation. Here, we use multi-dimensional genomic associations to assess the basis of local and climate adaptation in two sympatric, cryptic Crematogaster levior ant species along a climate gradient. Additionally, we investigate the genomic basis of chemical communication in both species. Communication in insects is mainly mediated by cuticular hydrocarbons (CHCs), which also protect against water loss and, hence, are subject to changes via environmental acclimation or adaptation. The combination of environmental and chemical association analyses based on genome-wide Pool-Seq data allowed us to identify single nucleotide polymorphisms (SNPs) associated with climate and with chemical differences. Within species, CHC changes as a response to climate seem to be driven by phenotypic plasticity, since there is no overlap between climate- and CHC-associated SNPs. The only exception is the odorant receptor OR22c, which may be a candidate for population-specific CHC recognition in one of the species. Within both species, climate is significantly correlated with CHC differences, as well as to allele frequency differences. However, associated candidate SNPs, genes and functions are largely species-specific and we find evidence for minimal parallel evolution only on the level of genomic regions (J=0.04). This highlights that even closely related species may follow divergent evolutionary trajectories when expressing similar adaptive phenotypes.

Molecular signatures of local adaptation to light in Norway spruce

Main conclusionTranscriptomic and exome capture analysis reveal an adaptive cline for shade tolerance in Norway spruce. Genes involved in the lignin pathway and immunity seem to play a potential role in contributing towards local adaptation to light.The study of natural variation is an efficient method to elucidate how plants adapt to local climatic conditions, a key process for the evolution of a species. Norway spruce is a shade-tolerant conifer in which the requirement of far-red light for growth increases latitudinally northwards. The objective of the study is to characterize the genetic control of local adaptation to light enriched in far-red in Norway spruce, motivated by a latitudinal gradient for the Red:Far-red (R:FR) ratio to which Norway spruce has been proven to be genetically adapted. We have established the genomic signatures of local adaptation by conducting transcriptomic (total RNA-sequencing) and genomic analyses (exome capture), for the identification of genes differentially regulated along the cline. RNA-sequencing revealed 274 differentially expressed genes in response to SHADE (low R:FR light), between the southern and northern natural populations in Sweden. Exome capture included analysis of a uniquely large data set (1654 trees) that revealed missense variations in coding regions of nine differentially expressed candidate genes, which followed a latitudinal cline in allele and genotype frequencies. These genes included five transcription factors involved in vital processes like bud-set/bud-flush, lignin pathway, and cold acclimation and other genes that take part in cell-wall remodeling, secondary cell-wall thickening, response to starvation, and immunity. Based on these results, we suggest that the northern populations might not only be able to adjust their growing season in response to low R:FR light, but they may also be better adapted towards disease resistance by up-regulation of the lignin pathway that is linked to immunity. This forms a concrete basis for local adaptation to light quality in Norway spruce, one of the most economically important conifer tree species in Sweden.

Victoria L. Sork—Recipient of the 2020 Molecular Ecology Prize

Victoria L. Sork—Recipient of the 2020 Molecular Ecology Prize

Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, in Drosophila melanogaster.

Organisms living in seasonally variable environments utilize cues such as light and temperature to induce plastic responses, enabling them to exploit favorable seasons and avoid unfavorable ones. Local adapation can result in variation in seasonal responses, but the genetic basis and evolutionary history of this variation remains elusive. Many insects, including Drosophila melanogaster, are able to undergo an arrest of reproductive development (diapause) in response to unfavorable conditions. In D. melanogaster, the ability to diapause is more common in high latitude populations, where flies endure harsher winters, and in the spring, reflecting differential survivorship of overwintering populations. Using a novel hybrid swarm-based genome wide association study, we examined the genetic basis and evolutionary history of ovarian diapause. We exposed outbred females to different temperatures and day lengths, characterized ovarian development for over 2800 flies, and reconstructed their complete, phased genomes. We found that diapause, scored at two different developmental cutoffs, has modest heritability, and we identified hundreds of SNPs associated with each of the two phenotypes. Alleles associated with one of the diapause phenotypes tend to be more common at higher latitudes, but these alleles do not show predictable seasonal variation. The collective signal of many small-effect, clinally varying SNPs can plausibly explain latitudinal variation in diapause seen in North America. Alleles associated with diapause are segregating in Zambia, suggesting that variation in diapause relies on ancestral polymorphisms, and both pro- and anti-diapause alleles have experienced selection in North America. Finally, we utilized outdoor mesocosms to track diapause under natural conditions. We found that hybrid swarms reared outdoors evolved increased propensity for diapause in late fall, whereas indoor control populations experienced no such change. Our results indicate that diapause is a complex, quantitative trait with different evolutionary patterns across time and space.

Adaptation, ancestral variation and gene flow in a 'Sky Island' Drosophila species.

Over time, populations of species can expand, contract, fragment and become isolated, creating subpopulations that must adapt to local conditions. Understanding how species maintain variation after divergence as well as adapt to these changes in the face of gene flow is of great interest, especially as the current climate crisis has caused range shifts and frequent migrations for many species. Here, we characterize how a mycophageous fly species, Drosophila innubila, came to inhabit and adapt to its current range which includes mountain forests in south-western USA separated by large expanses of desert. Using population genomic data from more than 300 wild-caught individuals, we examine four populations to determine their population history in these mountain forests, looking for signatures of local adaptation. In this first extensive study, establishing D.innubila as a key genomic "Sky Island" model, we find D.innubila spread northwards during the previous glaciation period (30-100KYA) and have recently expanded even further (0.2-2KYA). D.innubila shows little evidence of population structure, consistent with a recent establishment and genetic variation maintained since before geographic stratification. We also find some signatures of recent selective sweeps in chorion proteins and population differentiation in antifungal immune genes suggesting differences in the environments to which flies are adapting. However, we find little support for long-term recurrent selection in these genes. In contrast, we find evidence of long-term recurrent positive selection in immune pathways such as the Toll signalling system and the Toll-regulated antimicrobial peptides.

Molecular and Fitness Data Reveal Local Adaptation of Southern and Northern Estuarine Oysters (Crassostrea ariakensis)

Natural selection and genetic drift are both important for understanding the geographic distribution and environmental responses of marine species. In this study, we revealed distinct genetic variation in Crassostrea ariakensis by comparing the COI gene segment sequence in northern and southern oysters separated by the Yangtze River estuary. Reciprocal hybridization and intrapopulation crosses clarified their taxonomic status as the same species. There was no heterosis in the survival and growth of the hybrids, while the maternal effect was observed in larvae from eggs in the native habitat that showed higher fitness. Both the northern and southern F1 progenies exhibited positive performance in fitness traits, including survivorship, respiration rate, and growth, in their native habitats compared to that in their non-native habitats, indicating a strong signature of local adaptation. The oysters dwelling in the warm/southern habitats evolved a higher thermotolerance of LT50, while the oysters inhabiting the high-salinity/northern habitats had a 2.43‰ higher LS50 than that of their southern counterparts. After strong natural selection in the northern environments, the higher survival of the F1 progenies from the southern oysters under heat shock indicates an evolved genetic basis for its higher thermal tolerance. Strong environmental gradients, especially for temperature and salinity, and genetic drift of the interaction between coastal currents and the Yangtze River estuary potentially contribute to shaping the distribution pattern and adaptive divergence of C. ariakensis in China.

Population Genetic Structure and Gene Expression Plasticity of the Deep-Sea Vent and Seep Squat Lobster Shinkaia crosnieri

Shinkaia crosnieri (Munidopsidae) is a squat lobster that dominates both deep-sea hydrothermal vent and methane seep communities in the Western Pacific. Previous studies comparing S. crosnieri living in the two types of habitats have suffered from methodological and/or sample size limits. Here, using transcriptome-wide genetic markers from 44 individuals, we reveal the extent of genetic connectivity between a population of S. crosnieri collected from a methane seep in the South China Sea (SCS) and another collected from a hydrothermal vent in the Okinawa Trough (OT), as well as their signatures of local adaptation. Analysis of differentially expressed genes (DEGs) between these two populations and analysis of population-specific genes (PSGs) revealed that a great number of unigenes, such as cytochrome P450 (CYP), glutathione S-transferase (GST) and peroxiredoxin 6 (Prdx6) related to oxidoreductase, and sulfur dioxygenase (ETHE1) and chondroitin 4-sulfotransferase 11 (CHST11) related to sulfur metabolism, showed opposite expression patterns in these two populations. Data subsampling revealed that at least five individuals per site are required to generate reliable results from differential gene expression analysis. Population genetic analyses based on 32,452 single-nucleotide polymorphisms (SNPs) revealed clear genetic differentiation between these two populations with an FST value of 0.07. Analysis of outlier SNPs revealed 345 unigenes potentially under positive selection, such as sarcosine oxidase/L-pipecolate oxidase (PIPOX), alanine-glyoxylate transaminase/serine-glyoxylate transaminase/serine-pyruvate transaminase (AGXT), and Cu-Zn superoxide dismutase (SOD1). Different gene expressions and amino acid substitutions of some genes between the two sites related to oxidation resistance and xenobiotic detoxification may indicate adaptation to the specific environmental conditions of each site. Overall, exploring the population structure of S. crosnieri using transcriptome-wide SNP markers resulted in an improved understanding of its molecular adaptation and expression plasticity in vent and seep ecosystems.

Genomic Prediction of (Mal)Adaptation Across Current and Future Climatic Landscapes

Signals of local adaptation have been found in many plants and animals, highlighting the heterogeneity in the distribution of adaptive genetic variation throughout species ranges. In the coming decades, global climate change is expected to induce shifts in the selective pressures that shape this adaptive variation. These changes in selective pressures will likely result in varying degrees of local climate maladaptation and spatial reshuffling of the underlying distributions of adaptive alleles. There is a growing interest in using population genomic data to help predict future disruptions to locally adaptive gene-environment associations. One motivation behind such work is to better understand how the effects of changing climate on populations’ short-term fitness could vary spatially across species ranges. Here we review the current use of genomic data to predict the disruption of local adaptation across current and future climates. After assessing goals and motivationsunderlying the approach, we review the main steps and associated statistical methods currently in use and explore our current understanding of the limits and future potential of using genomics to predict climate change (mal)adaptation.

Modern Strategies to Assess and Breed Forest Tree Adaptation to Changing Climate.

Studying the genetics of adaptation to new environments in ecologically and industrially important tree species is currently a major research line in the fields of plant science and genetic improvement for tolerance to abiotic stress. Specifically, exploring the genomic basis of local adaptation is imperative for assessing the conditions under which trees will successfully adapt in situ to global climate change. However, this knowledge has scarcely been used in conservation and forest tree improvement because woody perennials face major research limitations such as their outcrossing reproductive systems, long juvenile phase, and huge genome sizes. Therefore, in this review we discuss predictive genomic approaches that promise increasing adaptive selection accuracy and shortening generation intervals. They may also assist the detection of novel allelic variants from tree germplasm, and disclose the genomic potential of adaptation to different environments. For instance, natural populations of tree species invite using tools from the population genomics field to study the signatures of local adaptation. Conventional genetic markers and whole genome sequencing both help identifying genes and markers that diverge between local populations more than expected under neutrality, and that exhibit unique signatures of diversity indicative of “selective sweeps.” Ultimately, these efforts inform the conservation and breeding status capable of pivoting forest health, ecosystem services, and sustainable production. Key long-term perspectives include understanding how trees’ phylogeographic history may affect the adaptive relevant genetic variation available for adaptation to environmental change. Encouraging “big data” approaches (machine learning—ML) capable of comprehensively merging heterogeneous genomic and ecological datasets is becoming imperative, too.

Balancing selection versus allele and supertype turnover in MHC class II genes in guppies.

Selection pressure from parasites is thought to be a major force shaping the extreme polymorphism of the major histocompatibility complex (MHC) genes, but the modes and consequences of selection remain unclear. Here, we analyse MHC class II and microsatellite diversity in 16 guppy (Poecilia reticulata) populations from two islands (Trinidad and Tobago) that have been separated for at least 10 ky. Within-population MHC diversity was high, but allele sharing was limited within islands and even lower between islands, suggesting relatively fast turnover of alleles. Allelic lineages strongly supported in phylogenetic analyses tended to be island-specific, suggesting rapid lineage sorting, and an expansion of an allelic lineage private to Tobago was observed. New alleles appear to be generated locally at a detectably high frequency. We did not detect a consistent signature of local adaptation, but FST outlier analysis suggested that balancing selection may be the more general process behind spatial variation in MHC allele frequencies in this system, particularly within Trinidad. We found no evidence for divergent allele advantage within populations, or for decreased genetic structuring of MHC supertypes compared to MHC alleles. The dynamic and complex nature of MHC evolution we observed in guppies, coupled with some evidence for balancing selection shaping MHC allele frequencies, are consistent with Red Queen processes of host-parasite coevolution.

Association of genetic and climatic variability in giant sequoia, Sequoiadendron giganteum, reveals signatures of local adaptation along moisture-related gradients.

Uncovering the genetic basis of local adaptation is a major goal of evolutionary biology and conservation science alike. In an era of climate change, an understanding of how environmental factors shape adaptive diversity is crucial to predicting species response and directing management. Here, we investigate patterns of genomic variation in giant sequoia, an iconic and ecologically important tree species, using 1,364 bi‐allelic single nucleotide polymorphisms (SNPs). We use an F ST outlier test and two genotype–environment association methods, latent factor mixed models (LFMMs) and redundancy analysis (RDA), to detect complex signatures of local adaptation. Results indicate 79 genomic regions of potential adaptive importance, with limited overlap between the detection methods. Of the 58 loci detected by LFMM, 51 showed strong correlations to a precipitation‐driven composite variable and seven to a temperature‐related variable. RDA revealed 24 outlier loci with association to climate variables, all of which showed strongest relationship to summer precipitation. Nine candidate loci were indicated by two methods. After correcting for geographic distance, RDA models using climate predictors accounted for 49% of the explained variance and showed significant correlations between SNPs and climatic factors. Here, we present evidence of local adaptation in giant sequoia along gradients of precipitation and provide a first step toward identifying genomic regions of adaptive significance. The results of this study will provide information to guide management strategies that seek to maximize adaptive potential in the face of climate change.

Signatures of local adaptation in the spatial genetic structure of the ascidian Pyura chilensis along the southeast Pacific coast

The highly heterogeneous Humboldt Current System (HCS) and the 30°S transition zone on the southeast Pacific coast, represent an ideal scenario to test the influence of the environment on the spatial genomic structure in marine near-shore benthic organisms. In this study, we used seascape genomic tools to evaluate the genetic structure of the commercially important ascidian Pyura chilensis, a species that exhibits a low larval transport potential but high anthropogenic dispersal. A recent study in this species recorded significant genetic differentiation across a transition zone around 30°S in putatively adaptive SNPs, but not in neutral ones, suggesting an important role of environmental heterogeneity in driving genetic structure. Here, we aim to understand genomic-oceanographic associations in P. chilensis along the Southeastern Pacific coast using two combined seascape genomic approaches. Using 149 individuals from five locations along the HCS, a total of 2,902 SNPs were obtained by Genotyping-By-Sequencing, of which 29–585 were putatively adaptive loci, depending on the method used for detection. In adaptive loci, spatial genetic structure was better correlated with environmental differences along the study area (mainly to Sea Surface Temperature, upwelling-associated variables and productivity) than to the geographic distance between sites. Additionally, results consistently showed the presence of two groups, located north and south of 30°S, which suggest that local adaptation processes seem to allow the maintenance of genomic differentiation and the spatial genomic structure of the species across the 30°S biogeographic transition zone of the Humboldt Current System, overriding the homogenizing effects of gene flow.

Shared ancestral polymorphisms and chromosomal rearrangements as potential drivers of local adaptation in a marine fish.

Gene flow has tremendous importance for local adaptation, by influencing the fate of de novo mutations, maintaining standing genetic variation and driving adaptive introgression. Furthermore, structural variation as chromosomal rearrangements may facilitate adaptation despite high gene flow. However, our understanding of the evolutionary mechanisms impending or favouring local adaptation in the presence of gene flow is still limited to a restricted number of study systems. In this study, we examined how demographic history, shared ancestral polymorphism, and gene flow among glacial lineages contribute to local adaptation to sea conditions in a marine fish, the capelin (Mallotus villosus). We first assembled a 490-Mbp draft genome of M.villosus to map our RAD sequence reads. Then, we used a large data set of genome-wide single nucleotide polymorphisms (25,904 filtered SNPs) genotyped in 1,310 individuals collected from 31 spawning sites in the northwest Atlantic. We reconstructed the history of divergence among three glacial lineages and showed that they probably diverged from 3.8 to 1.8million years ago and experienced secondary contacts. Within each lineage, our analyses provided evidence for large Ne and high gene flow among spawning sites. Within the Northwest Atlantic lineage, we detected a polymorphic chromosomal rearrangement leading to the occurrence of three haplogroups. Genotype-environment associations revealed molecular signatures of local adaptation to environmental conditions prevailing at spawning sites. Our study also suggests that both shared polymorphisms among lineages, resulting from standing genetic variation or introgression, and chromosomal rearrangements may contribute to local adaptation in the presence of high gene flow.

Genomic Signatures of Local Adaptation in Clam Shrimp (Eulimnadia texana) from Natural Vernal Pools.

Vernal pools are unique in their isolation and the strong selection acting on their resident species. Vernal pool clam shrimp (Eulimnadia texana) are a promising model due to ease of culturing, short generation time, small genomes, and obligate desiccated diapaused eggs. Clam shrimp are also androdioecious (sexes include males and hermaphrodites), and here we use population-scaled recombination rates to support the hypothesis that the heterogametic sex is recombination free in these shrimp. We collected short-read sequence data from pooled samples from different vernal pools to gain insights into local adaptation. We identify genomic regions in which some populations have allele frequencies that differ significantly from the metapopulation. BayPass (Gautier M. 2015. Genome-wide scan for adaptive divergence and association with population-specific covariates. Genetics 201(4):1555–1579.) detected 19 such genomic regions showing an excess of population subdivision. These regions on average are 550 bp in size and had 2.5 genes within 5 kb of them. Genes located near these regions are involved in Malpighian tubule function and osmoregulation, an essential function in vernal pools. It is likely that salinity profiles vary between pools and over time, and variants at these genes are adapted to local salinity conditions.

Effects of landscapes and range expansion on population structure and local adaptation.

Understanding the origin and distribution of genetic diversity across landscapes is critical for predicting the future of organisms in changing climates. This study investigated how adaptive and demographic forces have shaped diversity and population structure in Pinus densata, a keystone species on Qinghai-Tibetan Plateau (QTP). We examined the distribution of genomic diversity across the range of P.densata using exome capture sequencing. We applied spatially explicit tests to dissect the impacts of allele surfing, geographic isolation and environmental gradients on population differentiation and forecasted how this genetic legacy may limit the persistence of P.densata in future climates. We found that allele surfing from range expansion could explain the distribution of 39% of the c. 48000 genotyped single nucleotide polymorphisms (SNPs). Uncorrected, these allele frequency clines severely confounded inferences of selection. After controlling for demographic processes, isolation-by-environment explained 9.2-19.5% of the genetic structure, with c. 4.0% of loci being affected by selection. Allele surfing and genotype-environment associations resulted in genomic mismatch under projected climate scenarios. We illustrate that significant local adaptation, when coupled with reduced diversity as a result of demographic history, constrains potential evolutionary response to climate change. The strong signal of genomic vulnerability in P.densata may be representative for other QTP endemics.