Adaptive Loci Research Articles

A brief history of population genetic research in California and an evaluation of its utility for conservation decision-making.

A recently published macrogenetic dataset of California's flora and fauna, CaliPopGen, comprehensively summarizes population genetic research published between 1985 and 2020. Integrating these genetic data into the requisite "best available science" upon which conservation professionals rely should facilitate the prioritization of populations based on genetic health. We evaluate the extent to which the CaliPopGen Dataset provides genetic diversity estimates that are 1) unbiased, 2) sufficient in quantity, 3) cover entire species' ranges, and 4) include potentially adaptive loci. We identified genetic diversity estimates for 4,462 spatially referenced populations of 432 species, confirming California's rich published history of population genetics research. Most recent studies used microsatellites markers, which have uniquely high levels of variation, and estimates of all genetic metrics varied significantly across marker types. Most studies used less than 10 loci for inferences, rendering parameter estimates potentially unreliable, and covered small spatial extents that include only a fraction of the studied species' California distribution (median 16.3%). In contrast, the ongoing California Conservation Genomics Project (CCGP) aims to cover the full geographical and environmental breadth of each species' occupied habitats, and uses a consistent approach based on whole-genome data. However, the CCGP will sequence only 12% of the number of individuals, and covers only about half the evolutionary diversity, of the CaliPopGen Database. There is clearly a place in the evaluation of the genetic health of California for both approaches going forward, especially if differences among studies can be minimized, and overlap emphasized. A complementary use of both datasets is warranted to inform optimal conservation decision-making. Finally, a synopsis of the available population genetic data for California, all other US states and 241 other countries, allows us to identify states and countries for which meaningful data summaries, such as CaliPopGen, could be collated and others, which have limited published data available and are prime targets for future, empirical work.

Sexual imprinting leads to speciation in locally adapted populations.

Sexual imprinting is widespread in birds and other species but its existence requires explanation. Our results suggest that sexual imprinting leads to speciation in locally-adapted populations if a neutral mating cue-e.g., novel plumage coloration-arises through mutation. Importantly, the mating cue locus is not linked to adaptation loci. Local adaptation is a necessary precursor to speciation and occurs when evolution results in stable genetic polymorphisms with one allele predominating in some areas while others predominate elsewhere. Here we use a deterministic two-niche population genetic model to map the set of migration and selection rates for which polymorphic evolutionary outcomes, i.e., local adaptations, can occur. Approximate equations for the boundaries of the set of polymorphic evolutionary outcomes were derived by Bulmer (American Naturalist, 106, 254, 1972), but our results, obtained by deterministic simulation of the evolutionary process, show that one of Bulmer's equations is inaccurate except when the level of dominance is 0.5, and fails if one of the alleles is dominant. Having an accurate map of the set of migration and selection rates for which polymorphic evolutionary outcomes can occur, we then show using the model of Sibly et al. (Ecology and Evolution, 9, 13506, 2019) that local adaptation in all analyzed cases leads to speciation if a new neutral mating cue arises by mutation. We finish by considering how genome sequencing makes possible testing our model and its predictions.

Characterizing wild germplasm of neglected and underutilized crops: A case study of pomegranate (Punica granatum L.) from remote Pir Panjal Himalaya

Despite a wide range of nutritional and nutraceutical diversity existing within the wild germplasm of pomegranate (Punica granatum L.) that can be utilized to develop genetically superior cultivars, little research efforts have been focused on the characterization of this neglected and underutilized crop in the Himalaya. To fill this research gap, the present study carried out in the remote mountainous region of Pir Panjal Himalaya aimed to characterize the morphological variability, assess the genetic variability and relationship among and between the different populations of wild pomegranate, and identify the elite genotype for future plant propagation. We observed significant differences among all the 18 morphological descriptors analyzed; fruit traits showed the highest power of discrimination among the wild pomegranate accessions. Based on ANOVA results, most of the morphological variables showed significant differences among the studied populations (p˂0.001). Further, redundancy analysis (RDA) revealed that only two fruit traits, the number of arils and aril weight showed a significant relationship within all the populations. Molecular characterization, based on ISSR marker analysis, showed substantial genetic diversity within and between the populations of wild pomegranate in this Himalayan region. In this regard, RDA identified one potentially adaptive locus that strongly affects the different populations of wild pomegranate. Analysis of molecular variance (AMOVA) revealed 58% variation among populations and 42% variation within populations. Our research findings, based on detailed morphological and molecular characterization, provide precious information on the genetic diversity of wild pomegranate. We have identified elite genotypes that can guide climate-smart agriculture based on local genetic resources in this remote Himalayan region.

Neutral and adaptive loci reveal fine-scale population structure in Eleginops maclovinus from north Patagonia.

Patagonia is an understudied area, especially when it comes to population genomic studies with relevance to fishery management. However, the dynamic and heterogeneous landscape in this area can harbor an important but cryptic genetic population structure. Once such information is revealed, it can be integrated into the management of infrequently investigated species. Eleginops maclovinus is a protandrous hermaphrodite species with economic importance for local communities that are currently managed as a single genetic unit. In this study, we sampled five locations distributed across a salinity cline from Northern Patagonia to investigate the genetic population structure of E. maclovinus. We used restriction site‐associated DNA (RAD) sequencing and outlier tests to obtain neutral and adaptive loci, using FST and GEA approaches. We identified a spatial pattern of structuration with gene flow and spatial selection by environmental association. Neutral and adaptive loci showed two and three genetic groups, respectively. The effective population sizes estimated ranged from 572 (Chepu) to 14,454 (Chaitén) and were influenced more by locality than by salinity cline. We found loci putatively associated with salinity suggesting that salinity may act as a selective driver in E. maclovinus populations. These results suggest a complex interaction between genetic drift, gene flow, and natural selection in this area. Our findings also suggest several evolutionary significant units in this area, and the information should be integrated into the management of this species. We discussed the significance of these results for fishery management and suggest future directions to improve our understanding of how E. maclovinus has adapted to the dynamic waters of Northern Patagonia.

Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis.

Sexual antagonism is a common hypothesis for driving the evolution of sex chromosomes, whereby recombination suppression is favored between sexually antagonistic loci and the sex‐determining locus to maintain beneficial combinations of alleles. This results in the formation of a sex‐determining region. Chromosomal inversions may contribute to recombination suppression but their precise role in sex chromosome evolution remains unclear. Because local adaptation is frequently facilitated through the suppression of recombination between adaptive loci by chromosomal inversions, there is potential for inversions that cover sex‐determining regions to be involved in local adaptation as well, particularly if habitat variation creates environment‐dependent sexual antagonism. With these processes in mind, we investigated sex determination in a well‐studied example of local adaptation within a species: the intertidal snail, Littorina saxatilis. Using SNP data from a Swedish hybrid zone, we find novel evidence for a female‐heterogametic sex determination system that is restricted to one ecotype. Our results suggest that four putative chromosomal inversions, two previously described and two newly discovered, span the putative sex chromosome pair. We determine their differing associations with sex, which suggest distinct strata of differing ages. The same inversions are found in the second ecotype but do not show any sex association. The striking disparity in inversion‐sex associations between ecotypes that are connected by gene flow across a habitat transition that is just a few meters wide indicates a difference in selective regime that has produced a distinct barrier to the spread of the newly discovered sex‐determining region between ecotypes. Such sex chromosome‐environment interactions have not previously been uncovered in L. saxatilis and are known in few other organisms. A combination of both sex‐specific selection and divergent natural selection is required to explain these highly unusual patterns.

Genomic analyses of rice bean landraces reveal adaptation and yield related loci to accelerate breeding

Rice bean (Vigna umbellata) is an underexploited domesticated legume crop consumed for dietary protein in Asia, yet little is known about the genetic diversity of this species. Here, we present a high-quality reference genome for a rice bean landrace (FF25) built using PacBio long-read data and a Hi-C chromatin interaction map, and assess the phylogenetic position and speciation time of rice bean within the Vigna genus. We sequence 440 landraces (two core collections), and GWAS based on data for growth sites at three widely divergent latitudes reveal loci associated with flowering and yield. Loci harboring orthologs of FUL (FRUITFULL), FT (FLOWERING LOCUS T), and PRR3 (PSEUDO-RESPONSE REGULATOR 3) contribute to the adaptation of rice bean from its low latitude center of origin towards higher latitudes, and the landraces which pyramid early-flowering alleles for these loci display maximally short flowering times. We also demonstrate that copy-number-variation for VumCYP78A6 can regulate seed-yield traits. Intriguingly, 32 landraces collected from a mountainous region in South-Central China harbor a recently acquired InDel in TFL1 (TERMINAL FLOWER1) affecting stem determinacy; these materials also have exceptionally high values for multiple human-desired traits and could therefore substantially advance breeding efforts to improve rice bean.

Pattern of Adaptive Divergence in Zingiber kawagoii Hayata (Zingiberaceae) along a Narrow Latitudinal Range.

Ecological and evolutionary processes linking adaptation to environment are related to species’ range shifts. In this study, we employed amplified-fragment-length-polymorphism-based genome scan methods to identify candidate loci among Zingiber kawagoii populations inhabiting varying environments distributed at low to middle elevations (143–1488 m) in a narrow latitudinal range (between 21.90 and 25.30° N). Here, we show evidence of selection driving the divergence of Z. kawagoii. Twenty-six FST outliers were detected, which were significantly correlated with various environmental variables. The allele frequencies of nine FST outliers were either positively or negatively correlated with the population mean FST. Using several independent approaches, we found environmental variables act in a combinatorial fashion, best explaining outlier genetic variation. Nonetheless, we found that adaptive divergence was affected mostly by annual temperature range, and it is significantly positively correlated with latitude and significantly negatively correlated with the population mean FST. This study addresses a latitudinal pattern of changes in annual temperature range (which ranged from 13.8 °C in the Lanyu population to 18.5 °C in the Wulai population) and emphasizes the pattern of latitudinal population divergence closely linked to the allele frequencies of adaptive loci, acting in a narrow latitudinal range. Our results also indicate environmentally dependent local adaptation for both leading- and trailing-edge populations.

High-density genomic data reveal fine-scale population structure and pronounced islands of adaptive divergence in lake whitefish (Coregonus clupeaformis) from Lake Michigan.

Understanding patterns of genetic structure and adaptive variation in natural populations is crucial for informing conservation and management. Past genetic research using 11 microsatellite loci identified six genetic stocks of lake whitefish (Coregonus clupeaformis) within Lake Michigan, USA. However, ambiguity in genetic stock assignments suggested those neutral microsatellite markers did not provide adequate power for delineating lake whitefish stocks in this system, prompting calls for a genomics approach to investigate stock structure. Here, we generated a dense genomic dataset to characterize population structure and investigate patterns of neutral and adaptive genetic diversity among lake whitefish populations in Lake Michigan. Using Rapture sequencing, we genotyped 829 individuals collected from 17 baseline populations at 197,588 SNP markers after quality filtering. Although the overall pattern of genetic structure was similar to the previous microsatellite study, our genomic data provided several novel insights. Our results indicated a large genetic break between the northwestern and eastern sides of Lake Michigan, and we found a much greater level of population structure on the eastern side compared to the northwestern side. Collectively, we observed five genomic islands of adaptive divergence on five different chromosomes. Each island displayed a different pattern of population structure, suggesting that combinations of genotypes at these adaptive regions are facilitating local adaptation to spatially heterogenous selection pressures. Additionally, we identified a large linkage disequilibrium block of ~8.5Mb on chromosome 20 that is suggestive of a putative inversion but with a low frequency of the minor haplotype. Our study provides a comprehensive assessment of population structure and adaptive variation that can help inform the management of Lake Michigan's lake whitefish fishery and highlights the utility of incorporating adaptive loci into fisheries management.

Bray-Curtis (AFD) differentiation in molecular ecology: Forecasting, an adjustment ( A A), and comparative performance in selection detection.

Geographic genetic differentiation measures are used for purposes such as assessing genetic diversity and connectivity, and searching for signals of selection. Confirmation by unrelated measures can minimize false positives. A popular differentiation measure, Bray‐Curtis, has been used increasingly in molecular ecology, renamed AFD (hereafter called BCAFD). Critically, BCAFD is expected to be partially independent of the commonly used Hill “Q‐profile” measures. BCAFD needs scrutiny for potential biases, by examining limits on its value, and comparing simulations against expectations. BCAFD has two dependencies on within‐population (alpha) variation, undesirable for a between‐population (beta) measure. The first dependency is derived from similarity to GST and FST. The second dependency is that BCAFD cannot be larger than the highest allele proportion in either location (alpha variation), which can be overcome by data‐filtering or by a modified statistic A A or “Adjusted AFD”. The first dependency does not forestall applications such as assessing connectivity or selection, if we know the measure's null behavior under selective neutrality with specified conditions—which is shown in this article for A A, for equilibrium, and nonequilibrium, for the commonly used data type of single‐nucleotide‐polymorphisms (SNPs) in two locations. Thus, A A can be used in tandem with mathematically contrasting differentiation measures, with the aim of reducing false inferences. For detecting adaptive loci, the relative performance of A A and other measures was evaluated, showing that it is best to use two mathematically different measures simultaneously, and that A A is in one of the best such pairwise criteria. For any application, using A A, rather than BCAFD, avoids the counterintuitive limitation by maximum allele proportion within localities.

Landscape genomics of the American lobster (Homarus americanus).

In marine species experiencing intense fishing pressures, knowledge of genetic structure and local adaptation represent a critical information to assist sustainable management. In this study, we performed a landscape genomics analysis in the American lobster to investigate the issues pertaining to the consequences of making use of putative adaptive loci to reliably infer population structure and thus more rigorously delineating biological management units in marine exploited species. Toward this end, we genotyped 14,893 single nucleotide polymorphism (SNPs) in 4190 lobsters sampled across 96 sampling sites distributed along 1000 km in the northwest Atlantic in both Canada and the USA. As typical for most marine species, we observed a weak, albeit highly significant genetic structure. We also found that adaptive genetic variation allows detecting fine-scale population structure not resolved by neutral genetic variation alone. Using the recent genome assembly of the American lobster, we were able to map and annotate several SNPs located in functional genes potentially implicated in adaptive processes such as thermal stress response, salinity tolerance and growth metabolism pathways. Taken together, our study indicates that weak population structure in high gene flow systems can be resolved at various spatial scales, and that putatively adaptive genetic variation can substantially enhance the delineation of biological management units of marine exploited species.

Distinct evolutionary trajectories of SARS-CoV-2-interacting proteins in bats and primates identify important host determinants of COVID-19

The coronavirus disease 19 (COVID-19) pandemic is caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), a coronavirus that spilled over from the bat reservoir. Despite numerous clinical trials and vaccines, the burden remains immense, and the host determinants of SARS-CoV-2 susceptibility and COVID-19 severity remain largely unknown. Signatures of positive selection detected by comparative functional genetic analyses in primate and bat genomes can uncover important and specific adaptations that occurred at virus-host interfaces. We performed high-throughput evolutionary analyses of 334 SARS-CoV-2-interacting proteins to identify SARS-CoV adaptive loci and uncover functional differences between modern humans, primates, and bats. Using DGINN (Detection of Genetic INNovation), we identified 38 bat and 81 primate proteins with marks of positive selection. Seventeen genes, including the ACE2 receptor, present adaptive marks in both mammalian orders, suggesting common virus-host interfaces and past epidemics of coronaviruses shaping their genomes. Yet, 84 genes presented distinct adaptations in bats and primates. Notably, residues involved in ubiquitination and phosphorylation of the inflammatory RIPK1 have rapidly evolved in bats but not primates, suggesting different inflammation regulation versus humans. Furthermore, we discovered residues with typical virus-host arms race marks in primates, such as in the entry factor TMPRSS2 or the autophagy adaptor FYCO1, pointing to host-specific invivo interfaces that may be drug targets. Finally, we found that FYCO1 sites under adaptation in primates are those associated with severe COVID-19, supporting their importance in pathogenesis and replication. Overall, we identified adaptations involved in SARS-CoV-2 infection in bats and primates, enlightening modern genetic determinants of virus susceptibility and severity.

Pollinator loss causes rapid adaptive evolution of selfing and dramatically reduces genome-wide genetic variability.

Although selfing populations harbor little genetic variation limiting evolutionary potential, the causes are unclear. We experimentally evolved large, replicate populations of Mimulus guttatus for nine generations in greenhouses with or without pollinating bees and studied DNA polymorphism in descendants. Populations without bees adapted to produce more selfed seed yet exhibited striking reductions in DNA polymorphism despite large population sizes. Importantly, the genome‐wide pattern of variation cannot be explained by a simple reduction in effective population size, but instead reflects the complicated interaction between selection, linkage, and inbreeding. Simulations demonstrate that the spread of favored alleles at few loci depresses neutral variation genome wide in large populations containing fully selfing lineages. It also generates greater heterogeneity among chromosomes than expected with neutral evolution in small populations. Genome‐wide deviations from neutrality were documented in populations with bees, suggesting widespread influences of background selection. After applying outlier tests to detect loci under selection, two genome regions were found in populations with bees, yet no adaptive loci were otherwise mapped. Large amounts of stochastic change in selfing populations compromise evolutionary potential and undermine outlier tests for selection. This occurs because genetic draft in highly selfing populations makes even the largest changes in allele frequency unremarkable.

Interspecies genome divergence is predominantly due to frequent small scale rearrangements in Eucalyptus.

Synteny, the ordering of sequences within homologous chromosomes, must be maintained within the genomes of sexually reproducing species for the sharing of alleles and production of viable, reproducing offspring. However, when the genomes of closely related species are compared, a loss of synteny is often observed. Unequal homologous recombination is the primary mechanism behind synteny loss, occurring more often in transposon rich regions, and resulting in the formation of chromosomal rearrangements. To examine patterns of synteny among three closely related, interbreeding, and wild Eucalyptus species, we assembled their genomes using long-read DNA sequencing and de novo assembly. We identify syntenic and rearranged regions between these genomes and estimate that ~48% of our genomes remain syntenic while ~36% is rearranged. We observed that rearrangements highly fragment microsynteny. Our results suggest that synteny between these species is primarily lost through small-scale rearrangements, not through sequence loss, gain, or sequence divergence. Further examination of identified rearrangements suggests that rearrangements may be altering the phenotypes of Eucalyptus species. Our study also underscores that the use of single reference genomes in genomic variation studies could lead to reference bias, especially given the scale at which we show potentially adaptive loci have highly diverged, deleted, duplicated and/or rearranged. This study provides an unbiased framework to look at potential speciation and adaptive loci among a rapidly radiating foundation species of woodland trees that are free from selective breeding seen in most crop species.

Alternative Modes of Introgression-Mediated Selection Shaped Crop Adaptation to Novel Climates.

Recent plant genomic studies provide fine-grained details on the evolutionary consequences of adaptive introgression during crop domestication. Modern genomic approaches and analytical methods now make it possible to better separate the introgression signal from the demographic signal thus providing a more comprehensive and complex picture of the role of introgression in local adaptation. Adaptive introgression has been fundamental for crop expansion and has involved complex patterns of gene flow. In addition to providing new and more favorable alleles of large effect, introgression during the early stages of domestication also increased allelic diversity at adaptive loci. Previous studies have largely underestimated the effect of such increased diversity following introgression. Recent genomic studies in wheat, potato, maize, grapevine, and ryegrass show that introgression of multiple genes, of as yet unknown effect, increased the effectiveness of purifying selection, and promoted disruptive or fluctuating selection in early cultivars and landraces. Historical selection processes associated with introgression from crop wild relatives provide an instructive analog for adaptation to current climate change and offer new avenues for crop breeding research that are expected to be instrumental for strengthening food security in the coming years.

Genetics of adaptation

The rediscovery of Mendel’s work showing that the heredity of phenotypes is controlled by discrete genes was followed by the reconciliation of Mendelian genetics with evolution by natural selection in the middle of the last century with the Modern Synthesis. In the past two decades, dramatic advances in genomic methods have facilitated the identification of the loci, genes, and even individual mutations that underlie phenotypic variants that are the putative targets of natural selection. Moreover, these methods have also changed how we can study adaptation by flipping the problem around, allowing us to first examine what loci show evidence of having been under selection, and then connecting these genetic variants to phenotypic variation. As a result, we now have an expanding list of actual genetic changes that underlie potentially adaptive phenotypic variation. Here, we synthesize how considering the effects of these adaptive loci in the context of cellular environments, genomes, organisms, and populations has provided new insights to the genetic architecture of adaptation.

Genetic diversity and connectivity of chemosynthetic cold seep mussels from the U.S. Atlantic margin

BackgroundDeep-sea mussels in the subfamily Bathymodiolinae have unique adaptations to colonize hydrothermal-vent and cold-seep environments throughout the world ocean. These invertebrates function as important ecosystem engineers, creating heterogeneous habitat and promoting biodiversity in the deep sea. Despite their ecological significance, efforts to assess the diversity and connectivity of this group are extremely limited. Here, we present the first genomic-scale diversity assessments of the recently discovered bathymodioline cold-seep communities along the U.S. Atlantic margin, dominated by Gigantidas childressi and Bathymodiolus heckerae.ResultsA Restriction-site Associated DNA Sequencing (RADSeq) approach was used on 177 bathymodiolines to examine genetic diversity and population structure within and between seep sites. Assessments of genetic differentiation using single-nucleotide polymorphism (SNP) data revealed high gene flow among sites, with the shallower and more northern sites serving as source populations for deeper occurring G. childressi. No evidence was found for genetic diversification across depth in G. childressi, likely due to their high dispersal capabilities. Kinship analyses indicated a high degree of relatedness among individuals, and at least 10–20% of local recruits within a particular site. We also discovered candidate adaptive loci in G. childressi and B. heckerae that suggest differences in developmental processes and depth-related and metabolic adaptations to chemosynthetic environments.ConclusionsThese results highlight putative source communities for an important ecosystem engineer in the deep sea that may be considered in future conservation efforts. Our results also provide clues into species-specific adaptations that enable survival and potential speciation within chemosynthetic ecosystems.

Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci.

Supergenes are genetic architectures associated with discrete and concerted variation in multiple traits. It has long been suggested that supergenes control these complex polymorphisms by suppressing recombination between sets of coadapted genes. However, because recombination suppression hinders the dissociation of the individual effects of genes within supergenes, there is still little evidence that supergenes evolve by tightening linkage between coadapted genes. Here, combining a landmark-free phenotyping algorithm with multivariate genome-wide association studies, we dissected the genetic basis of wing pattern variation in the butterfly Heliconius numata. We show that the supergene controlling the striking wing pattern polymorphism displayed by this species contains several independent loci associated with different features of wing patterns. The three chromosomal inversions of this supergene suppress recombination between these loci, supporting the hypothesis that they may have evolved because they captured beneficial combinations of alleles. Some of these loci are, however, associated with colour variations only in a subset of morphs where the phenotype is controlled by derived inversion forms, indicating that they were recruited after the formation of the inversions. Our study shows that supergenes and clusters of adaptive loci in general may form via the evolution of chromosomal rearrangements suppressing recombination between co-adapted loci but also via the subsequent recruitment of linked adaptive mutations. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.

Hybrid enrichment of adaptive variation revealed by genotype-environment associations in montane sedges.

The role of hybridization in diversification is complex and may result in many possible outcomes. Not only can hybridization produce new lineages, but those lineages may contain unique combinations of adaptive genetic variation derived from parental taxa that allow hybrid‐origin lineages to occupy unique environmental space relative to one (or both) parent(s). We document such a case of hybridization between two sedge species, Carex nova and Carex nelsonii (Cyperaceae), that occupy partially overlapping environmental space in the southern Rocky Mountains, USA. In the region hypothesized to be the origin of the hybrid lineage, one parental taxon (C. nelsonii) is at the edge of its environmental tolerance. Hybrid‐origin individuals display mixed ancestry between the parental taxa—of nearly 7000 unlinked loci sampled, almost 30% showed evidence of excess ancestry from one parental lineage—approximately half displayed a genomic background skewed towards one parent, and half skewed towards the other. To test whether excess ancestry loci may have conferred an adaptive advantage to the hybrid‐origin lineage, we conducted genotype–environment association analyses on different combinations of loci—with and without excess ancestry—and with multiple contrasts between the hybrids and parental taxa. Loci with skewed ancestry showed significant environmental associations distinguishing the hybrid lineage from one parent (C. nelsonii), whereas loci with relatively equal representation of parental ancestries showed no such environmental associations. Moreover, the overwhelming majority of candidate adaptive loci with respect to environmental gradients also had excess ancestry from a parental lineage, implying these loci have facilitated the persistence of the hybrid lineage in an environment unsuitable to at least one parent.

Testing for fitness epistasis in a transplant experiment identifies a candidate adaptive locus in Timema stick insects.

Identifying the genetic basis of adaptation is a central goal of evolutionary biology. However, identifying genes and mutations affecting fitness remains challenging because a large number of traits and variants can influence fitness. Selected phenotypes can also be difficult to know a priori, complicating top-down genetic approaches for trait mapping that involve crosses or genome-wide association studies. In such cases, experimental genetic approaches, where one maps fitness directly and attempts to infer the traits involved afterwards, can be valuable. Here, we re-analyse data from a transplant experiment involving Timema stick insects, where five physically clustered single-nucleotide polymorphisms associated with cryptic body coloration were shown to interact to affect survival. Our analysis covers a larger genomic region than past work and revealed a locus previously not identified as associated with survival. This locus resides near a gene, Punch (Pu), involved in pteridine pigments production, implying that it could be associated with an unmeasured coloration trait. However, by combining previous and newly obtained phenotypic data, we show that this trait is not eye or body coloration. We discuss the implications of our results for the discovery of traits, genes and mutations associated with fitness in other systems, as well as for supergene evolution. This article is part of the theme issue 'Genetic basis of adaptation and speciation: from loci to causative mutations'.

Local Adaptation and the Evolution of Genome Architecture in Threespine Stickleback.

Theory predicts that local adaptation should favor the evolution of a concentrated genetic architecture, where the alleles driving adaptive divergence are tightly clustered on chromosomes. Adaptation to marine versus freshwater environments in threespine stickleback has resulted in an architecture that seems consistent with this prediction: divergence among populations is mainly driven by a few genomic regions harboring multiple quantitative trait loci for environmentally adapted traits, as well as candidate genes with well-established phenotypic effects. One theory for the evolution of these “genomic islands” is that rearrangements remodel the genome to bring causal loci into tight proximity, but this has not been studied explicitly. We tested this theory using synteny analysis to identify micro- and macro-rearrangements in the stickleback genome and assess their potential involvement in the evolution of genomic islands. To identify rearrangements, we conducted a de novo assembly of the closely related tubesnout (Aulorhyncus flavidus) genome and compared this to the genomes of threespine stickleback and two other closely related species. We found that small rearrangements, within-chromosome duplications, and lineage-specific genes (LSGs) were enriched around genomic islands, and that all three chromosomes harboring large genomic islands have experienced macro-rearrangements. We also found that duplicates and micro-rearrangements are 9.9× and 2.9× more likely to involve genes differentially expressed between marine and freshwater genotypes. While not conclusive, these results are consistent with the explanation that strong divergent selection on candidate genes drove the recruitment of rearrangements to yield clusters of locally adaptive loci.