Fine‐scale genetic structuring in a group‐living lizard,the gidgee skink (Egernia stokesii)

By constraining gene flow, group living and natal philopatry can result in fine‐scale genetic structure. Although the genetic structure of some group‐living lizards has been characterised, studies are few compared with those for group‐living bird and mammal species. The Egerniinae group of lizards exhibits a high diversity of social structures, making it a useful group for comparative studies of genetic structure across a broader range of social taxa. A well‐studied member of Egerniinae is Egernia stokesii, a lizard that forms long‐term pair bonds and stable social groups and exhibits natal philopatry and limited dispersal. Evidence exists for consistent E. stokesii social structure across seven close but disconnected rocky outcrops within a 40 × 10 km area. We used summary statistics, analysis of molecular variance, Bayesian clustering, and discriminant analysis of principal components to assess if E. stokesii exhibit a consistent pattern of fine‐scale genetic structure across the same seven outcrops. Due to E. stokesii social structure and constrained dispersal, we predicted significant genetic structuring – based on microsatellite markers – among outcrops. We found significant fine‐scale genetic structuring and evidence for two genetic clusters. We discuss features of E. stokesii biology and ecology that may explain our findings. Some rocky outcrops, and some social groups, contained lizards from both genetic clusters. An examination of the composition of mixed cluster social groups did not detect any notable patterns. Therefore, further work is necessary to identify how the observed patterns may have arisen. Future investigations in E. stokesii and other group‐living lizard species are likely to contribute greatly to our understanding of the genetic consequences of group living.     

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 F_ST 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 in situ and ex situ conservation management of biodiversity.     

High degree of genetic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus)

Populations of widespread marine organisms are typically characterized by a low degree of genetic differentiation in neutral genetic markers, but much less is known about differentiation in genes whose functional roles are associated with specific selection regimes. To uncover possible adaptive population divergence and heterogeneous genomic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus), we used a candidate gene‐based genome‐scan approach to analyse variability in 138 microsatellite loci located within/close to (<6 kb) functionally important genes in samples collected from ten geographic locations. The degree of genetic differentiation in markers classified as neutral or under balancing selection—as determined with several outlier detection methods—was low (F_ST = 0.033 or 0.011, respectively), whereas average F_ST for directionally selected markers was significantly higher (F_ST = 0.097). Clustering analyses provided support for genomic and geographic heterogeneity in selection: six genetic clusters were identified based on allele frequency differences in the directionally selected loci, whereas four were identified with the neutral loci. Allelic variation in several loci exhibited significant associations with environmental variables, supporting the conjecture that temperature and salinity, but not optic conditions, are important drivers of adaptive divergence among populations. In general, these results suggest that in spite of the high degree of physical connectivity and gene flow as inferred from neutral marker genes, marine stickleback populations are strongly genetically structured in loci associated with functionally relevant genes.     

Pathogen richness and abundance predict patterns of adaptive major histocompatibility complex variation in insular amphibians

The identification of the factors responsible for genetic variation and differentiation at adaptive loci can provide important insights into the evolutionary process and is crucial for the effective management of threatened species. We studied the impact of environmental viral richness and abundance on functional diversity and differentiation of the MHC class Ia locus in populations of the black‐spotted pond frog (Pelophylax nigromaculatus), an IUCN‐listed species, on 24 land‐bridge islands of the Zhoushan Archipelago and three nearby mainland sites. We found a high proportion of private MHC alleles in mainland and insular populations, corresponding to 32 distinct functional supertypes, and strong positive selection on MHC antigen‐binding sites in all populations. Viral pathogen diversity and abundance were reduced at island sites relative to the mainland, and islands housed distinctive viral communities. Standardized MHC diversity at island sites exceeded that found at neutral microsatellites, and the representation of key functional supertypes was positively correlated with the abundance of specific viruses in the environment (Frog virus 3 and Ambystoma tigrinum virus). These results indicate that pathogen‐driven diversifying selection can play an important role in maintaining functionally important MHC variation following island isolation, highlighting the importance of considering functionally important genetic variation and host–pathogen associations in conservation planning and management.     

Drift,selection and adaptive variation in small populations of a threatened rattlesnake

An important goal of conservation genetics is to determine if the viability of small populations is reduced by a loss of adaptive variation due to genetic drift. Here, we assessed the impact of drift and selection on direct measures of adaptive variation (toxin loci encoding venom proteins) in the eastern massasauga rattlesnake (Sistrurus catenatus), a threatened reptile that exists in small isolated populations. We estimated levels of individual polymorphism in 46 toxin loci and 1,467 control loci across 12 populations of this species, and compared the results with patterns of selection on the same loci following speciation of S. catenatus and its closest relative, the western massasauga (S. tergeminus). Multiple lines of evidence suggest that both drift and selection have had observable impacts on standing adaptive variation. In support of drift effects, we found little evidence for selection on toxin variation within populations and a significant positive relationship between current levels of adaptive variation and long‐ and short‐term estimates of effective population size. However, we also observed levels of directional selection on toxin loci among populations that are broadly similar to patterns predicted from interspecific selection analyses that pre‐date the effects of recent drift, and that functional variation in these loci persists despite small short‐term effective sizes. This suggests that much of the adaptive variation present in populations may represent an example of “drift debt,” a nonequilibrium state where present‐day levels of variation overestimate the amount of functional genetic diversity present in future populations.     

On the relative roles of selection and genetic drift in shaping MHC variation

Genes of the major histocompatibility complex (MHC) have provided some of the clearest examples of how natural selection generates discordances between adaptive and neutral variation in natural populations. The type and intensity of selection as well as the strength of genetic drift are believed to be important in shaping the resulting pattern of MHC diversity. However, evaluating the relative contribution of multiple microevolutionary forces is challenging, and empirical studies have reported contrasting results. For instance, balancing selection has been invoked to explain high levels of MHC diversity and low population differentiation in comparison with other nuclear markers. Other studies have shown that genetic drift can sometimes overcome selection and then patterns of genetic variation at adaptive loci cannot be discerned from those occurring at neutral markers. Both empirical and simulated data also indicate that loss of genetic diversity at adaptive loci can occur faster than at neutral loci when selection and population bottlenecks act simultaneously. Diversifying selection, on the other hand, explains accelerated MHC divergence as the result of spatial variation in pathogen‐mediated selective regimes. Because of all these possible scenarios and outcomes, collecting information from as many study systems as possible, is crucial to enhance our understanding about the evolutionary forces driving MHC polymorphism. In this issue, Miller and co‐workers present an illuminating contribution by combining neutral markers (microsatellites) and adaptive MHC class I loci during the investigation of genetic differentiation across island populations of tuatara Sphenodon punctatus. Their study of geographical variation reveals a major role of genetic drift in shaping MHC variation, yet they also discuss some support for diversifying selection.     

On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system

Dispersal and natural selection are key evolutionary processes shaping the distribution of phenotypic and genetic diversity. For species inhabiting complex spatial environments however, it is unclear how the balance between gene flow and selection may be influenced by landscape heterogeneity and environmental variation. Here, we evaluated the effects of dendritic landscape structure and the selective forces of hydroclimatic variation on population genomic parameters for the Murray River rainbowfish, Melanotaenia fluviatilis across the Murray–Darling Basin, Australia. We genotyped 249 rainbowfish at 17,503 high‐quality SNP loci and integrated these with models of network connectivity and high‐resolution environmental data within a riverscape genomics framework. We tested competing models of gene flow before using multivariate genotype–environment association (GEA) analysis to test for signals of adaptive divergence associated with hydroclimatic variation. Patterns of neutral genetic variation were consistent with expectations based on the stream hierarchy model and M. fluviatilis’ moderate dispersal ability. Models incorporating dendritic network structure suggested that landscape heterogeneity is a more important factor determining connectivity and gene flow than waterway distance. Extending these results, we also introduce a novel approach to controlling for the unique effects of dendritic network structure in GEA analyses of populations of aquatic species. We identified 146 candidate loci potentially underlying a polygenic adaptive response to seasonal fluctuations in stream flow and variation in the relative timing of temperature and precipitation extremes. Our findings underscore an emerging predominant role for seasonal variation in hydroclimatic conditions driving local adaptation and are relevant for informing proactive conservation management.     

Spatial and temporal patterns of neutral and adaptive genetic variation in the endangered African wild dog (Lycaon pictus)

Deciphering patterns of genetic variation within a species is essential for understanding population structure, local adaptation and differences in diversity between populations. Whilst neutrally evolving genetic markers can be used to elucidate demographic processes and genetic structure, they are not subject to selection and therefore are not informative about patterns of adaptive variation. As such, assessments of pertinent adaptive loci, such as the immunity genes of the major histocompatibility complex (MHC), are increasingly being incorporated into genetic studies. In this study, we combined neutral (microsatellite, mtDNA) and adaptive (MHC class II DLA‐DRB1 locus) markers to elucidate the factors influencing patterns of genetic variation in the African wild dog (Lycaon pictus); an endangered canid that has suffered extensive declines in distribution and abundance. Our genetic analyses found all extant wild dog populations to be relatively small (N_e < 30). Furthermore, through coalescent modelling, we detected a genetic signature of a recent and substantial demographic decline, which correlates with human expansion, but contrasts with findings in some other African mammals. We found strong structuring of wild dog populations, indicating the negative influence of extensive habitat fragmentation and loss of gene flow between habitat patches. Across populations, we found that the spatial and temporal structure of microsatellite diversity and MHC diversity were correlated and strongly influenced by demographic stability and population size, indicating the effects of genetic drift in these small populations. Despite this correlation, we detected signatures of selection at the MHC, implying that selection has not been completely overwhelmed by genetic drift.     

Local adaptation through genetic differentiation in highly fragmented Tilia cordata populations

We assessed the level of geographic differentiation of Tilia cordata in Denmark based on tests of 91 trees selected from 12 isolated populations. We used quantitative analysis of spring phenology and population genetic analysis based on SSR markers to infer the likely historical genetic processes within and among populations. High genetic variation within and among populations was observed in spring phenology, which correlated with spring temperatures at the origin of the tested T. cordata trees. The population genetic analysis revealed significant differentiation among the populations, but with no clear sign of isolation by distance. We infer the findings as indications of ongoing fine scale selection in favor of local growth conditions made possible by limited gene flow among the small and fragmented populations. This hypothesis fits well with reports of limited fruiting in the investigated Danish T. cordata populations, while the species is known for its ability to propagate vegetatively by root suckers. Our results suggest that both divergent selection and genetic drift may have played important roles in forming the genetic patterns of T. cordata at its northern distribution limit. However, we also speculate that epigenetic mechanism arising from the original population environment could have created similar patterns in regulating the spring phenology.     

Cunningham's skinks show low genetic connectivity and signatures of divergent selection across its distribution

Establishing corridors of connecting habitat has become a mainstay conservation strategy to maintain gene flow and facilitate climate‐driven range shifts. Yet, little attention has been given to ascertaining the extent to which corridors will benefit philopatric species, which might exhibit localized adaptation. Measures of genetic connectivity and adaptive genetic variation across species’ ranges can help fill this knowledge gap. Here, we characterized the spatial genetic structure of Cunningham's skink (Egernia cunninghami), a philopatric species distributed along Australia's Great Dividing Range, and assessed evidence of localized adaptation. Analysis of 4,274 SNPs from 94 individuals sampled at four localities spanning 500 km and 4° of latitude revealed strong genetic structuring at neutral loci (mean F_ST ± SD = 0.603 ± 0.237) among the localities. Putatively neutral SNPs and those under divergent selection yielded contrasting spatial patterns, with the latter identifying two genetically distinct clusters. Given low genetic connectivity of the four localities, we suggest that the natural movement rate of this species is insufficient to keep pace with spatial shifts to its climate envelope, irrespective of habitat availability. In addition, our finding of localized adaptation highlights the risk of outbreeding depression should the translocation of individuals be adopted as a conservation management strategy.     

Investigation of the geographical scale of adaptive phenological variation and its underlying genetics in Arabidopsis thaliana

Despite the increasing number of genomic tools, identifying the genetics underlying adaptive complex traits remains challenging in the model species Arabidopsis thaliana. This is due, at least in part, to the lack of data on the geographical scale of adaptive phenotypic variation. The aims of this study were (i) to tease apart the historical roles of adaptive and nonselective processes in shaping phenological variation in A. thaliana in France and (ii) to gain insights into the spatial scale of adaptive variation by identifying the putative selective agents responsible for this selection. Forty‐nine natural stands from four climatically contrasted French regions were characterized (i) phenologically for six traits, (ii) genetically using 135 SNP markers and (iii) ecologically for 42 variables. Up to 63% of phenological variation could be explained by neutral genetic diversity. The remaining phenological variation displayed stronger associations with ecological variation within regions than among regions, suggesting the importance of local selective agents in shaping adaptive phenological variation. Although climatic conditions have often been suggested as the main selective agents acting on phenology in A. thaliana, both edaphic conditions and interspecific competition appear to be strong selective agents in some regions. In a first attempt to identify the genetics of phenological variation at different geographical scales, we phenotyped worldwide accessions and local polymorphic populations from the French RegMap in a genome‐wide association (GWA) mapping study. The genomic regions associated with phenological variation depended upon the geographical scale considered, stressing the need to account for the scale of adaptive phenotypic variation when choosing accession panels for GWAS.     

Genetic analysis of differentiation among breeding ponds reveals a candidate gene for local adaptation in Rana arvalis

One of the main questions in evolutionary and conservation biology is how geographical and environmental features of the landscape shape neutral and adaptive genetic variation in natural populations. The identification of genomic polymorphisms that account for adaptive variation can aid in finding candidate loci for local adaptation. Consequently, a comparison of spatial patterns in neutral markers and loci under selection may help disentangle the effects of gene flow, genetic drift and selection at the landscape scale. Many amphibians breed in wetlands, which differ in environmental conditions and in the degree of isolation, enhancing the potential for local adaptation. We used microsatellite markers to measure genetic differentiation among 17 local populations of Rana arvalis breeding in a network of wetlands. We found that locus RC08604 deviated from neutral expectations, suggesting that it is a good candidate for directional selection. We used a genetic network analysis to show that the allele distribution in this locus is correlated with habitat characteristics, whereas this was not the case at neutral markers that displayed a different allele distribution and population network in the study area. The graph approach illustrated the genomic heterogeneity (neutral loci vs. the candidate locus for directional selection) of gene exchange and genetic divergence among populations under directional selection. Limited gene flow between wetlands was only observed at the candidate genomic region under directional selection. RC08604 is partially located inside an up‐regulated thyroid‐hormone receptor (TRβ) gene coordinating the expression of other genes during metamorphosis and appears to be linked with variation in larval life‐history traits found among R. arvalis populations. We suggest that directional selection on genes coding larval life‐history traits is strong enough to maintain the divergence in these genomic regions, reducing the effective recombination of locally adapted alleles but not in other regions of the genome. Integrating this knowledge into conservation plans at the landscape scale will improve the design of management strategies to preserve adaptive genetic diversity in wetland networks.     

Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection

Elucidating the adaptive genetic potential of wildlife populations to environmental selective pressures is fundamental for species conservation. Genes of the major histocompatibility complex (MHC) are highly polymorphic, and play a key role in the adaptive immune response against pathogens. MHC polymorphism has been linked to balancing selection or heterogeneous selection promoting local adaptation. However, spatial patterns of MHC polymorphism are also influenced by gene flow and drift. Wolverines are highly vagile, inhabiting varied ecoregions that include boreal forest, taiga, tundra, and high alpine ecosystems. Here, we investigated the immunogenetic variation of wolverines in Canada as a surrogate for identifying local adaptation by contrasting the genetic structure at MHC relative to the structure at 11 neutral microsatellites to account for gene flow and drift. Evidence of historical positive selection was detected at MHC using maximum likelihood codon-based methods. Bayesian and multivariate cluster analyses revealed weaker population genetic differentiation at MHC relative to the increasing microsatellite genetic structure towards the eastern wolverine distribution. Mantel correlations of MHC against geographical distances showed no pattern of isolation by distance (IBD: r = -0.03, p = 0.9), whereas for microsatellites we found a relatively strong and significant IBD (r = 0.54, p = 0.01). Moreover, we found a significant correlation between microsatellite allelic richness and the mean number of MHC alleles, but we did not observe low MHC diversity in small populations. Overall these results suggest that MHC polymorphism has been influenced primarily by balancing selection and to a lesser extent by neutral processes such as genetic drift, with no clear evidence for local adaptation. This study contributes to our understanding of how vulnerable populations of wolverines may respond to selective pressures across their range.     

Fine‐grained adaptive divergence in an amphibian: genetic basis of phenotypic divergence and the role of nonrandom gene flow in restricting effective migration among wetlands

Adaptive ecological differentiation among sympatric populations is promoted by environmental heterogeneity, strong local selection and restricted gene flow. High gene flow, on the other hand, is expected to homogenize genetic variation among populations and therefore prevent local adaptation. Understanding how local adaptation can persist at the spatial scale at which gene flow occurs has remained an elusive goal, especially for wild vertebrate populations. Here, we explore the roles of natural selection and nonrandom gene flow (isolation by breeding time and habitat choice) in restricting effective migration among local populations and promoting generalized genetic barriers to neutral gene flow. We examined these processes in a network of 17 breeding ponds of the moor frog Rana arvalis, by combining environmental field data, a common garden experiment and data on variation in neutral microsatellite loci and in a thyroid hormone receptor (TRβ) gene putatively under selection. We illustrate the connection between genotype, phenotype and habitat variation and demonstrate that the strong differences in larval life history traits observed in the common garden experiment can result from adaptation to local pond characteristics. Remarkably, we found that haplotype variation in the TRβ gene contributes to variation in larval development time and growth rate, indicating that polymorphism in the TRβ gene is linked with the phenotypic variation among the environments. Genetic distance in neutral markers was correlated with differences in breeding time and environmental differences among the ponds, but not with geographical distance. These results demonstrate that while our study area did not exceed the scale of gene flow, ecological barriers constrained gene flow among contrasting habitats. Our results highlight the roles of strong selection and nonrandom gene flow created by phenological variation and, possibly, habitat preferences, which together maintain genetic and phenotypic divergence at a fine‐grained spatial scale.     

Host‐associated genomic differentiation in congeneric butterflies: now you see it,now you do not

Ecotypic variation among populations may become associated with widespread genomic differentiation, but theory predicts that this should happen only under particular conditions of gene flow, selection and population size. In closely related species, we might expect the strength of host‐associated genomic differentiation (HAD) to be correlated with the degree of phenotypic differentiation in host‐adaptive traits. Using microsatellite and Amplified Fragment Length Polymorphism (AFLP) markers, and controlling for isolation by distance between populations, we sought HAD in two congeneric species of butterflies with different degrees of host plant specialization. Prior work on Euphydryas editha had shown strong interpopulation differentiation in host‐adapted traits, resulting in incipient reproductive isolation among host‐associated ecotypes. We show here that Euphydryas aurinia had much weaker host‐associated phenotypic differentiation. Contrary to our expectations, we detected HAD in Euphydryas aurinia, but not in E. editha. Even within an E. aurinia population that fed on both hosts, we found weak but significant sympatric HAD that persisted in samples taken 9 years apart. The finding of significantly stronger HAD in the system with less phenotypic differentiation may seem paradoxical. Our findings can be explained by multiple factors, ranging from differences in dispersal or effective population size, to spatial variation in genomic or phenotypic traits and to structure induced by past histories of host‐adapted populations. Other infrequently measured factors, such as differences in recombination rates, may also play a role. Our result adds to recent work as a further caution against assumptions of simple relationships between genomic and adaptive phenotypic differentiation.     

Molecular divergence in tropical tree populations occupying environmental mosaics

Unveiling the genetic basis of local adaptation to environmental variation is a major goal in molecular ecology. In rugged landscapes characterized by environmental mosaics, living populations and communities can experience steep ecological gradients over very short geographical distances. In lowland tropical forests, interspecific divergence in edaphic specialization (for seasonally flooded bottomlands and seasonally dry terra firme soils) has been proven by ecological studies on adaptive traits. Some species are nevertheless capable of covering the entire span of the gradient; intraspecific variation for adaptation to contrasting conditions may explain the distribution of such ecological generalists. We investigated whether local divergence happens at small spatial scales in two stands of Eperua falcata (Fabaceae), a widespread tree species of the Guiana Shield. We investigated Single Nucleotide Polymorphisms (SNP) and sequence divergence as well as spatial genetic structure (SGS) at four genes putatively involved in stress response and three genes with unknown function. Significant genetic differentiation was observed among sub‐populations within stands, and eight SNP loci showed patterns compatible with disruptive selection. SGS analysis showed genetic turnover along the gradients at three loci, and at least one haplotype was found to be in repulsion with one habitat. Taken together, these results suggest genetic differentiation at small spatial scale in spite of gene flow. We hypothesize that heterogeneous environments may cause molecular divergence, possibly associated to local adaptation in E. falcata.     

Clonal Diversity and Fine‐scale Genetic Structure in a High Andean Treeline Population

Clonal propagation becomes more abundant with increasing altitudes as environmental conditions worsen. To date, little attention has been paid to the way in which clonal propagation affects genetic diversity and the fine‐scale spatial genetic structure (FSGS) of clonal alpine trees. An AFLP study was undertaken to quantify the clonal and genetic diversity and FSGS of the vulnerable treeline species Polylepis reticulata in Ecuador. We successfully genotyped 32 and 75 ramets within 4 m × 100 m (coarse scale) and 4 m × 4 m (fine scale) transects of one population, respectively. Higher genotypic diversity was detected at the coarse scale than at the fine scale, while lower genetic diversity was detected for P. reticulata than other Polylepis spp. at both scales. Significantly stronger FSGS was detected at the ramet level than the genet level for P. reticulata within a spatial distance of 3 m. The studied P. reticulata population showed pronounced FSGS (Sp = 0.012 at the genet level, a statistic reflecting declining pairwise kinship with distance) revealed restricted gene dispersal, which implies restricted seed dispersal for this population, assuming pollen flow is as extensive as that described for other wind‐pollinated tree species. Our results revealed that clonal diversity is a function of both sample size and the spatial scale of the sampling area. The findings highlights that clonal propagation has affected FSGS within a spatial distance of 3 m for this species.     

Genetic drift outweighs natural selection at toll‐like receptor (TLR) immunity loci in a re‐introduced population of a threatened species

During population establishment, genetic drift can be the key driver of changes in genetic diversity, particularly while the population is small. However, natural selection can also play a role in shaping diversity at functionally important loci. We used a well‐studied, re‐introduced population of the threatened Stewart Island robin (N = 722 pedigreed individuals) to determine whether selection shaped genetic diversity at innate immunity toll‐like receptor (TLR) genes, over a 9‐year period of population growth following establishment with 12 genetic founders. We found no evidence for selection operating with respect to TLR diversity on first‐year overwinter survival for the majority of loci, genotypes and alleles studied. However, survival of individuals with TLR4_BE genotype was significantly improved: these birds were less than half as likely to die prior to maturity compared with all other TLR4 genotypes. Furthermore, the population frequency of this genotype, at a two‐fold excess over Hardy–Weinberg expectation, was increased by nonrandom mating. Near‐complete sampling and full pedigree and reproductive data enabled us to eliminate other potential causes of these patterns including inbreeding, year effects, density dependence, selection on animals at earlier life history stages or genome‐level association of the TLR4_E allele with ‘good genes’. However, comparison of observed levels of gene diversity to predictions under simulated genetic drift revealed results consistent with neutral expectations for all loci, including TLR4. Although selection favoured TLR4_BE heterozygotes in this population, these effects were insufficient to outweigh genetic drift. This is the first empirical study to show that genetic drift can overwhelm natural selection in a wild population immediately following establishment.     

Adaptation in temporally variable environments: stickleback armor in periodically breaching bar‐built estuaries

The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar‐built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re‐form within a few weeks or months, thereby re‐isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within‐population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure and then analysed how stickleback armor traits, the associated genes Eda and Pitx1 and elemental composition (%P) varies within and among populations. Despite strong gene flow, we detected evidence for divergence in stickleback defensive traits and Eda genotypes associated with predation regime. However, this among‐population variation was lower than that observed among other stickleback populations exposed to divergent predator regimes. In addition, within‐population variation was very high as compared to populations from environmentally stable locations. Elemental composition was strongly associated with armor traits, Eda genotype and the presence of predators, thus suggesting that spatiotemporal variation in armor traits generates corresponding variation in elemental phenotypes. We conclude that gene flow, and especially temporal environmental variation, can maintain high levels of within‐population variation while reducing, but not eliminating, among‐population variation driven by spatial environmental variation.     

Genetic depletion at adaptive but not neutral loci in an endangered bird species

Many endangered species suffer from the loss of genetic diversity, but some populations may be able to thrive even if genetically depleted. To investigate the underlying genetic processes of population bottlenecks, we apply an innovative approach for assessing genetic diversity in the last known population of the endangered Pale‐headed Brushfinch (Atlapetes pallidiceps) in Ecuador. First, we measure genetic diversity at eleven neutral microsatellite loci and adaptive SNP variation in five Toll‐like receptor (TLR) immune system genes. Bottleneck tests confirm genetic drift as the main force shaping genetic diversity in this species and indicate a 99 % reduction in population size dating back several hundred years. Second, we compare contemporary microsatellite diversity with historic museum samples of A. pallidiceps, finding no change in genetic diversity. Third, we compare genetic diversity in the Pale‐headed Brushfinch with two co‐occurring‐related brushfinch species (Atlapetes latinuchus, Buarremon torquatus), finding a reduction of up to 91% diversity in the immune system genes but not in microsatellites. High TLR diversity is linked to decreased survival probabilities in A. pallidiceps. Low TLR diversity is thus probably an adaptation to the specific selection regime within its currently very restricted distribution (approximately 200 ha), but could severely restrict the adaptive potential of the species in the long run. Our study illustrates the importance of investigating both neutral and adaptive markers to assess the effect of population bottlenecks and for recommending specific management plans in endangered species.