Genotype-environment Association Research Articles

Effects of Gene Action, Marker Density, and Timing of Selection on the Performance of Landscape Genomic Scans of Local Adaptation.

Genomic "scans" to identify loci that contribute to local adaptation are becoming increasingly common. Many methods used for such studies have assumed that local adaptation is created by loci experiencing antagonistic pleiotropy (AP) and that the selected locus itself is assayed, and few consider how signals of selection change through time. However, most empirical data sets have marker density too low to assume that a selected locus itself is assayed, researchers seldom know when selection was first imposed, and many locally adapted loci likely experience not AP but conditional neutrality (CN). We simulated data to evaluate how these factors affect the performance of tests for genotype-environment association (GEA). We found that 3 types of regression-based analyses (linear models, mixed linear models, and latent factor mixed models) and an implementation of BayEnv all performed well, with high rates of true positives and low rates of false positives, when the selected locus experienced AP, and when the selected locus was assayed directly. However, all tests had reduced power to detect loci experiencing CN, and the probability of detecting associations was sharply reduced when physically linked rather than causative loci were sampled. AP also maintained detectable GEAs much longer than CN. Our analyses suggest that if local adaptation is often driven by loci experiencing CN, genome-scan methods will have limited capacity to find loci responsible for local adaptation.

Genetic and genomic evidence of niche partitioning and adaptive radiation in mountain pine beetle fungal symbionts

Bark beetles form multipartite symbiotic associations with blue stain fungi (Ophiostomatales, Ascomycota). These fungal symbionts play an important role during the beetle's life cycle by providing nutritional supplementation, overcoming tree defences and modifying host tissues to favour brood development. The maintenance of stable multipartite symbioses with seemingly less competitive symbionts in similar habitats is of fundamental interest to ecology and evolution. We tested the hypothesis that the coexistence of three fungal species associated with the mountain pine beetle is the result of niche partitioning and adaptive radiation using SNP genotyping coupled with genotype-environment association analysis and phenotypic characterization of growth rate under different temperatures. We found that genetic variation and population structure within each species is best explained by distinct spatial and environmental variables. We observed both common (temperature seasonality and the host species) and distinct (drought, cold stress, precipitation) environmental and spatial factors that shaped the genomes of these fungi resulting in contrasting outcomes. Phenotypic intraspecific variations in Grosmannia clavigera and Leptographium longiclavatum, together with high heritability, suggest potential for adaptive selection in these species. By contrast, Ophiostoma montium displayed narrower intraspecific variation but greater tolerance to extreme high temperatures. Our study highlights unique phenotypic and genotypic characteristics in these symbionts that are consistent with our hypothesis. By maintaining this multipartite relationship, the bark beetles have a greater likelihood of obtaining the benefits afforded by the fungi and reduce the risk of being left aposymbiotic. Complementarity among species could facilitate colonization of new habitats and survival under adverse conditions.

Candidate gene variation in gilthead sea bream reveals complex spatiotemporal selection patterns between marine and lagoon habitats

In marine fishes, the extent to which spatial patterns induced by selection remain stable across generations remains largely unknown. In the gilthead sea bream (Sparus aurata), polymorphisms in the growth hormone (GH) and prolactin (Prl) genes can display high levels of differentiation between marine and lagoon habitats. These genotype-environment associations have been attributed to differential selection following larval settlement, but it remains unclear whether selective mortality during later juvenile stages further shapes genetic differences among habitats. We addressed this question by analysing differentiation patterns at GH and Prl markers together with a set of twenty-one putatively neutral microsatellite loci. We compared genetic variation of spring juveniles that had just settled in three ecologically different lagoons, against older juveniles sampled from the same sites in autumn, at the onset of winter outmigration. In spring, genetic differentiation among lagoons was greater than expected from neutrality, for both candidate gene markers. Surprisingly, this signal disappeared completely in the older juveniles, with no significant differentiation for either locus a few months later in autumn. We searched for signals of haplotype structure within GH and Prl genes using next-generation amplicon deep-sequencing. Both genes contained two groups of haplotypes, but high similarities among groups indicated that signatures of selection, if any, had largely been erased by recombination. Our results are consistent with the view that differential selection operates during early juvenile life in sea bream, and highlight the importance of temporal replication in studies of post-settlement selection in marine fish.

Riverscape genomics of a threatened fish across a hydroclimatically heterogeneous river basin.

Understanding how natural selection generates and maintains adaptive genetic diversity in heterogeneous environments is key to predicting the evolutionary response of populations to rapid environmental change. Detecting selection in complex spatial environments remains challenging, especially for threatened species where the effects of strong genetic drift may overwhelm signatures of selection. We carried out a basinwide riverscape genomic analysis in the threatened southern pygmy perch (Nannoperca australis), an ecological specialist with low dispersal potential. High-resolution environmental data and 5162 high-quality filtered SNPs were used to clarify spatial population structure and to assess footprints of selection associated with a steep hydroclimatic gradient and with human disturbance across the naturally and anthropogenically fragmented Murray-Darling Basin (Australia). Our approach included FST outlier tests to define neutral loci, and a combination of spatially explicit genotype-environment association analyses to identify candidate adaptive loci while controlling for the effects of landscape structure and shared population history. We found low levels of genetic diversity and strong neutral population structure consistent with expectations based on spatial stream hierarchy and life history. In contrast, variables related to precipitation and temperature appeared as the most important environmental surrogates for putatively adaptive genetic variation at both regional and local scales. Human disturbance also influenced the variation in candidate loci for adaptation, but only at a local scale. Our study contributes to understanding of adaptive evolution along naturally and anthropogenically fragmented ecosystems. It also offers a tangible example of the potential contributions of landscape genomics for informing insitu and ex situ conservation management of biodiversity.

Genotype-environment associations support a mosaic hybrid zone between two tidal marsh birds.

Local environmental features can shape hybrid zone dynamics when hybrids are bounded by ecotones or when patchily distributed habitat types lead to a corresponding mosaic of genotypes. We investigated the role of marsh-level characteristics in shaping a hybrid zone between two recently diverged avian taxa - Saltmarsh (Ammodramus caudacutus) and Nelson's (A.nelsoni) sparrows. These species occupy different niches where allopatric, with caudacutus restricted to coastal marshes and nelsoni found in a broader array of wetland and grassland habitats and co-occur in tidal marshes in sympatry. We determined the influence of habitat types on the distribution of pure and hybrid sparrows and assessed the degree of overlap in the ecological niche of each taxon. To do this, we sampled and genotyped 305 sparrows from 34 marshes across the hybrid zone and from adjacent regions. We used linear regression to test for associations between marsh characteristics and the distribution of pure and admixed sparrows. We found a positive correlation between genotype and environmental variables with a patchy distribution of genotypes and habitats across the hybrid zone. Ecological niche models suggest that the hybrid niche was more similar to that of A.nelsoni and habitat suitability was influenced strongly by distance from coastline. Our results support a mosaic model of hybrid zone maintenance, suggesting a role for local environmental features in shaping the distribution and frequency of pure species and hybrids across space.

Detecting spatial genetic signatures of local adaptation in heterogeneous landscapes.

The spatial structure of the environment (e.g. the configuration of habitat patches) may play an important role in determining the strength of local adaptation. However, previous studies of habitat heterogeneity and local adaptation have largely been limited to simple landscapes, which poorly represent the multiscale habitat structure common in nature. Here, we use simulations to pursue two goals: (i) we explore how landscape heterogeneity, dispersal ability and selection affect the strength of local adaptation, and (ii) we evaluate the performance of several genotype-environment association (GEA) methods for detecting loci involved in local adaptation. We found that the strength of local adaptation increased in spatially aggregated selection regimes, but remained strong in patchy landscapes when selection was moderate to strong. Weak selection resulted in weak local adaptation that was relatively unaffected by landscape heterogeneity. In general, the power of detection methods closely reflected levels of local adaptation. False-positive rates (FPRs), however, showed distinct differences across GEA methods based on levels of population structure. The univariate GEA approach had high FPRs (up to 55%) under limited dispersal scenarios, due to strong isolation by distance. By contrast, multivariate, ordination-based methods had uniformly low FPRs (0-2%), suggesting these approaches can effectively control for population structure. Specifically, constrained ordinations had the best balance of high detection and low FPRs and will be a useful addition to the GEA toolkit. Our results provide both theoretical and practical insights into the conditions that shape local adaptation and how these conditions impact our ability to detect selection.

Adoptive parent hostility and children’s peer behavior problems: Examining the role of genetically informed child attributes on adoptive parent behavior.

Socially disruptive behavior during peer interactions in early childhood is detrimental to children's social, emotional, and academic development. Few studies have investigated the developmental underpinnings of children's socially disruptive behavior using genetically sensitive research designs that allow examination of parent-on-child and child-on-parent (evocative genotype-environment correlation [rGE]) effects when examining family process and child outcome associations. Using an adoption-at-birth design, the present study controlled for passive genotype-environment correlation and directly examined evocative rGE while examining the associations between family processes and children's peer behavior. Specifically, the present study examined the evocative effect of genetic influences underlying toddler low social motivation on mother-child and father-child hostility and the subsequent influence of parent hostility on disruptive peer behavior during the preschool period. Participants were 316 linked triads of birth mothers, adoptive parents, and adopted children. Path analysis showed that birth mother low behavioral motivation predicted toddler low social motivation, which predicted both adoptive mother-child and father-child hostility, suggesting the presence of an evocative genotype-environment association. In addition, both mother-child and father-child hostility predicted children's later disruptive peer behavior. Results highlight the importance of considering genetically influenced child attributes on parental hostility that in turn links to later child social behavior. Implications for intervention programs focusing on early family processes and the precursors of disrupted child social development are discussed.

Microsatellite length variation in candidate genes correlates with habitat in the gilthead sea bream Sparus aurata

The genetic basis and evolutionary implications of local adaptation in high gene flow marine organisms are still poorly understood. In several Mediterranean fish species, alternative migration patterns exist between individuals entering coastal lagoons that offer favourable conditions for growth and those staying in the sea where environmental conditions are less subject to rapid and stressful change. Whether these coexisting strategies are phenotypically plastic or include a role for local adaptation through differential survival needs to be determined. Here, we explore the genetic basis of alternate habitat use in western Mediterranean populations of the gilthead sea bream (Sparus aurata). Samples from lagoonal and open-sea habitats were typed for three candidate gene microsatellite loci, seven anonymous microsatellites and 44 amplified fragment length polymorphism markers to test for genotype-environment associations. While anonymous markers globally indicated high levels of gene flow across geographic locations and habitats, non-neutral differentiation patterns correlated with habitat type were found at two candidate microsatellite loci located in the promoter region of the growth hormone and prolactin genes. Further analysis of these two genes revealed that a mechanism based on habitat choice alone could not explain the distribution of genotype frequencies at a regional scale, thus implying a role for differential survival between habitats. We also found an association between allele size and habitat type, which, in the light of previous studies, suggests that polymorphisms in the proximal promoter region could influence gene expression by modulating transcription factor binding, thus providing a potential explanatory link between genotype and growth phenotype in nature.

Detecting small‐scale genotype–environment interactions in apomictic dandelion (Taraxacum officinale) populations

Studies of genotype × environment interactions (G × E) and local adaptation provide critical tests of natural selection's ability to counter opposing forces such as gene flow. Such studies may be greatly facilitated in asexual species, given the possibility for experimental replication at the level of true genotypes (rather than populations) and the possibility of using molecular markers to assess genotype-environment associations in the field (neither of which is possible for most sexual species). Here, we tested for G × E in asexual dandelions (Taraxacum officinale) by subjecting six genotypes to experimental drought, mown and benign (control) conditions and subsequently using microsatellites to assess genotype-environment associations in the field. We found strong G × E, with genotypes that performed poorly under benign conditions showing the highest performance under stressful conditions (drought or mown). Our six focal genotypes comprise > 80% of plants in local populations. The most common genotype in the field showed its highest relative performance under mown conditions (the most common habitat in our study area), and almost all plants of this genotype in the field were found growing in mowed lawns. Genotypes performing best under benign experimental conditions were found most frequently in unmown conditions in the field. These results are strongly indicative of local adaptation at a very small scale, with unmown microsites of only a few square metres typically embedded within larger mown lawns. By studying an asexual species, we were able to map genotypes with known ecological characteristics to environments with high spatial precision.

Radiating on Oceanic Islands: Patterns and Processes of Speciation in the Land Snail Genus Theba (Risso 1826)

Island radiations have played a major role in shaping our current understanding of allopatric, sympatric and parapatric speciation. However, the fact that species divergence correlates with island size emphasizes the importance of geographic isolation (allopatry) in speciation. Based on molecular and morphological data, we investigated the diversification of the land snail genus Theba on the two Canary Islands of Lanzarote and Fuerteventura. Due to the geological history of both islands, this study system provides ideal conditions to investigate the interplay of biogeography, dispersal ability and differentiation in generating species diversity. Our analyses demonstrated extensive cryptic diversification of Theba on these islands, probably driven mainly by non-adaptive allopatric differentiation and secondary gene flow. In a few cases, we observed a complete absence of gene flow among sympatrically distributed forms suggesting an advanced stage of speciation. On the Jandía peninsula genome scans suggested genotype-environment associations and potentially adaptive diversification of two closely related Theba species to different ecological environments. We found support for the idea that genetic differentiation was enhanced by divergent selection in different environments. The diversification of Theba on both islands is therefore best explained by a mixture of non-adaptive and adaptive speciation, promoted by ecological and geomorphological factors.

Gene-environment correlations: a review of the evidence and implications for prevention of mental illness.

Family studies have demonstrated genetic influences on environmental exposure: the phenomenon of gene-environment correlation (rGE). A few molecular genetic studies have confirmed the results, but the identification of rGE in studies that measure genes and environments faces several challenges. Using examples from studies in psychology and psychiatry, we integrate the behavioral and molecular genetic literatures on rGE, describe challenges in identifying rGE and discuss the implications of molecular genetic findings of rGE for future research on gene-environment interplay and for attempts to prevent disease by reducing environmental risk exposure. Genes affect environments indirectly, via behavior and personality characteristics. Associations between individual genetic variants and behaviors are typically small in magnitude, and downstream effects on environmental risk are further attenuated by behavioral mediation. Genotype-environment associations are most likely to be detected when the environment is behaviorally modifiable and highly specified and a plausible mechanism links gene and behavior. rGEs play an important causal role in psychiatric illness. Although research efforts should concentrate on elucidating the genetic underpinnings of behavior rather than the environment itself, the identification of rGE may suggest targets for environmental intervention even in highly heritable disease. Prevention efforts must address the possibility of confounding between rGE and gene-environment interaction (G x E).

The developmental interface between nature and nurture: A mutual influence model of child antisocial behavior and parent behaviors.

Using an adoption design to collect data on biological and adoptive parents of children adopted at birth, this study explored a possible mechanism through which heritable characteristics of adopted children evoke adoptive parent responses and lead to reciprocal influences between adoptive parent and adopted child behavior. Participants were 25 male and 20 female adoptees, 12-18 years of age, having either a biological parent with substance abuse/dependency or antisocial personality or a biological parent with no such history. The study found that psychiatric disorders of biological parents were significantly related to children's antisocial/hostile behaviors and that biological parents' psychiatric disorders were associated with adoptive parents' behaviors. This genotype-environment association was largely mediated by adoptees' antisocial/hostile behaviors. Results also suggest that the adoptee's antisocial / hostile behavior and adoptive mother's parenting practices affect each other.