Adaptive landscape genetics: pitfalls and benefits

Landscape genetics offers a promising framework for assessing the interactions between the environment and adaptive genetic variation in natural populations. A recent workshop held at the University of Neuchatel brought together leading experts in this field to address current insights and future research directions in adaptive landscape genetics. Considerable amounts of genetic and/or environmental data can now be collected, but the forthcoming challenge is to do more with such manna. This requires a markedly better understanding of the genetic variation that is adaptive and prompts for advances in information management together with the development of a balance between theory and data. Moreover, showing the links between landscapes and adaptive genetic variation will ultimately move the field beyond association studies.     

The HLA‐B landscape of Africa: Signatures of pathogen‐driven selection and molecular identification of candidate alleles to malaria protection

Human leukocyte antigen (HLA) genes play a key role in the immune response to infectious diseases, some of which are highly prevalent in specific environments, like malaria in sub‐Saharan Africa. Former case–control studies showed that one particular HLA‐B allele, B*53, was associated with malaria protection in Gambia, but this hypothesis was not tested so far within a population genetics framework. In this study, our objective was to assess whether pathogen‐driven selection associated with malaria contributed to shape the HLA‐B genetic landscape of Africa. To that aim, we first typed the HLA‐A and ‐B loci in 484 individuals from 11 populations living in different environments across the Sahel, and we analysed these data together with those available for 29 other populations using several approaches including linear modelling on various genetic, geographic and environmental parameters. In addition to relevant signatures of populations’ demography and migrations history in the genetic differentiation patterns of both HLA‐A and ‐B loci, we found that the frequencies of three HLA alleles, B*53, B*78 and A*74, were significantly associated with Plasmodium falciparum malaria prevalence, suggesting their increase through pathogen‐driven selection in malaria‐endemic environments. The two HLA‐B alleles were further identified, by high‐throughput sequencing, as B*53:01:01 (in putative linkage disequilibrium with one HLA‐C allele, C*04:01:01:01) and B*78:01 in all but one individuals tested, making them appropriate candidates to malaria protection. These results highlight the role of environmental factors in the evolution of the HLA polymorphism and open key perspectives for functional studies focusing on HLA peptide‐binding properties.     

Adaptive phenotypic and genomic divergence in the common chaffinch (Fringilla coelebs) following niche expansion within a small oceanic island

According to models of ecological speciation, adaptation to adjacent, contrasting habitat types can lead to population divergence given strong enough environment-driven selection to counteract the homogenizing effect of gene flow. We tested this hypothesis in the common chaffinch (Fringilla coelebs) on the small island of La Palma, Canary Islands, where it occupies two markedly different habitats. Isotopic (δ¹³C, δ¹⁵N) analysis of feathers indicated that birds in the two habitats differed in ecosystem and/or diet, and analysis of phenotypic traits revealed significant differences in morphology and plumage colouration that are consistent with ecomorphological and ecogeographical predictions respectively. A genome-wide survey of single-nucleotide polymorphism revealed marked neutral structure that was consistent with geography and isolation by distance, suggesting low dispersal. In contrast, loci putatively under selection identified through genome-wide association and genotype-environment association analyses, revealed a marked adaptive divergence between birds in both habitats. Loci associated with phenotypic and environmental differences among habitats were distributed across the genome, as expected for polygenic traits involved in local adaptation. Our results suggest a strong role for habitat-driven local adaptation in population divergence in the chaffinches of La Palma, a process that appears to be facilitated by a strong reduction in effective dispersal distances despite the birds' high dispersal capacity.     

Population genetics of Anopheles koliensis through Papua New Guinea: New cryptic species and landscape topography effects on genetic connectivity

New Guinea is a topographically and biogeographically complex region that supports unique endemic fauna. Studies describing the population connectivity of species through this region are scarce. We present a population and landscape genetic study on the endemic malaria‐transmitting mosquito, Anopheles koliensis (Owen). Using mitochondrial and nuclear sequence data, as well as microsatellites, we show the evidence of geographically discrete population structure within Papua New Guinea (PNG). We also confirm the existence of three rDNA ITS2 genotypes within this mosquito and assess reproductive isolation between individuals carrying different genotypes. Microsatellites reveal the clearest population structure and show four clear population units. Microsatellite markers also reveal probable reproductive isolation between sympatric populations in northern PNG with different ITS2 genotypes, suggesting that these populations may represent distinct cryptic species. Excluding individuals belonging to the newly identified putative cryptic species (ITS2 genotype 3), we modeled the genetic differences between A. koliensis populations through PNG as a function of terrain and find that dispersal is most likely along routes with low topographic relief. Overall, these results show that A. koliensis is made up of geographically and genetically discrete populations in Papua New Guinea with landscape topography being important in restricting dispersal.     

Signatures of selection acting on the innate immunity gene Toll-like receptor 2 (TLR2) during the evolutionary history of rodents

Patterns of selection acting on immune defence genes have recently been the focus of considerable interest. Yet, when it comes to vertebrates, studies have mainly focused on the acquired branch of the immune system. Consequently, the direction and strength of selection acting on genes of the vertebrate innate immune defence remain poorly understood. Here, we present a molecular analysis of selection on an important receptor of the innate immune system of vertebrates, the Toll-like receptor 2 (TLR2), across 17 rodent species. Although purifying selection was the prevalent evolutionary force acting on most parts of the rodent TLR2, we found that codons in close proximity to pathogen-binding and TLR2-TLR1 heterodimerization sites have been subject to positive selection. This indicates that parasite-mediated selection is not restricted to acquired immune system genes like the major histocompatibility complex, but also affects innate defence genes. To obtain a comprehensive understanding of evolutionary processes in host-parasite systems, both innate and acquired immunity thus need to be considered.     

Waterscape genetics of the yellow perch ( Perca flavescens): patterns across large connected ecosystems and isolated relict populations

Comparisons of a species' genetic diversity and divergence patterns across large connected populations vs. isolated relict areas provide important data for understanding potential response to global warming, habitat alterations and other perturbations. Aquatic taxa offer ideal case studies for interpreting these patterns, because their dispersal and gene flow often are constrained through narrow connectivity channels that have changed over geological time and/or from contemporary anthropogenic perturbations. Our research objective is to better understand the interplay between historic influences and modern‐day factors (fishery exploitation, stocking supplementation and habitat loss) in shaping population genetic patterns of the yellow perch Perca flavescens (Percidae: Teleostei) across its native North American range. We employ a modified landscape genetics approach, analysing sequences from the entire mitochondrial DNA control region and 15 nuclear DNA microsatellite loci of 664 spawning adults from 24 populations. Results support that perch from primary glacial refugium areas (Missourian, Mississippian and Atlantic) founded contemporary northern populations. Genetic diversity today is highest in southern (never glaciated) populations and also is appreciable in northern areas that were founded from multiple refugia. Divergence is greater among isolated populations, both north and south; the southern Gulf Coast relict populations are the most divergent, reflecting their long history of isolation. Understanding the influence of past and current waterway connections on the genetic structure of yellow perch populations may help us to assess the roles of ongoing climate change and habitat disruptions towards conserving aquatic biodiversity.     

Genetic diversity and structuring across the range of a widely distributed ladybird: focus on rear‐edge populations phenotypically divergent

Population genetics and phenotypic structures are often predicted to vary along the geographic range of a species. This phenomenon would be accentuated for species with large range areas, with discontinuities and marginal populations. We herein compare the genetic patterns of central populations of Coccinella septempunctata L. with those of two phenotypically differentiated populations considered as rear‐edge populations and subspecies based on phenotype (Algeria and Japan). According to the central‐marginal model and expected characteristics of rear‐edge populations, we hypothesize that these rear‐edge populations have (1) a reduced genetic diversity, resulting from their relative isolation over long periods of time, (2) a higher population genetic differentiation, explained by low contemporary gene flow levels, and (3) a relationship between genetic diversity characteristics and phenotypes, due to historical isolation and/or local adaptation. Based on genotyping of 28 populations for 18 microsatellite markers, several levels of regional genetic diversity and differentiation are observed between and within populations, according to their localization: low within‐population genetic diversity and higher genetic differentiation of rear‐edge populations. The genetic structuring clearly dissociates the Algerian and Eastern Asia populations from the others. Geographical patterns of genetic diversity and differentiation support the hypothesis of the central‐marginal model. The pattern observed is in agreement with the phenotypic structure across species range. A clear genetic break between populations of Algeria, the Eastern Asia, and the remaining populations is a dominant feature of the data. Differential local adaptations, absence of gene flow between marginal and central populations, and/or incapacity to mate after colonization, have contributed to their distinct genotypic and phenotypic characteristics.     

Combining genome‐wide association study and FST‐based approaches to identify targets of Borrelia‐mediated selection in natural rodent hosts

Recent advances in high‐throughput sequencing technologies provide opportunities to gain novel insights into the genetic basis of phenotypic trait variation. Yet to date, progress in our understanding of genotype–phenotype associations in nonmodel organisms in general and natural vertebrate populations in particular has been hampered by small sample sizes typically available for wildlife populations and a resulting lack of statistical power, as well as a limited ability to control for false‐positive signals. Here we propose to combine a genome‐wide association study (GWAS) and F_ST‐based approach with population‐level replication to partly overcome these limitations. We present a case study in which we used this approach in combination with genotyping‐by‐sequencing (GBS) single nucleotide polymorphism (SNP) data to identify genomic regions associated with Borrelia afzelii resistance or susceptibility in the natural rodent host of this Lyme disease‐causing spirochete, the bank vole (Myodes glareolus). Using this combined approach we identified four consensus SNPs located in exonic regions of the genes Slc26a4, Tns3, Wscd1 and Espnl, which were significantly associated with the voles’ Borrelia infectious status within and across populations. Functional links between host responses to bacterial infections and most of these genes have previously been demonstrated in other rodent systems, making them promising new candidates for the study of evolutionary host responses to Borrelia emergence. Our approach is applicable to other systems and may facilitate the identification of genetic variants underlying disease resistance or susceptibility, as well as other ecologically relevant traits, in wildlife populations.     

Small‐scale spatial variation in infection risk shapes the evolution of a Borrelia resistance gene in wild rodents

Spatial variation in pathogen‐mediated selection is predicted to influence the evolutionary trajectory of host populations and lead to spatial variation in their immunogenetic composition. However, to date few studies have been able to directly link small‐scale spatial variation in infection risk to host immune gene evolution in natural, nonhuman populations. Here, we use a natural rodent–Borrelia system to test for associations between landscape‐level spatial variation in Borrelia infection risk along replicated elevational gradients in the Swiss Alps and Toll‐like receptor 2 (TLR2) evolution, a candidate gene for Borrelia resistance, across bank vole (Myodes glareolus) populations. We found that Borrelia infection risk (i.e., the product of Borrelia prevalence in questing ticks and the average tick load of voles at a sampling site) was spatially variable and significantly negatively associated with elevation. Across sampling sites, Borrelia prevalence in bank voles was significantly positively associated with Borrelia infection risk along the elevational clines. We observed a significant association between naturally occurring TLR2 polymorphisms in hosts and their Borrelia infection status. The TLR2 variant associated with a reduced likelihood of Borrelia infection was most common in rodent populations at lower elevations that face a high Borrelia infection risk, and its frequency changed in accordance with the change in Borrelia infection risk along the elevational clines. These results suggest that small‐scale spatial variation in parasite‐mediated selection affects the immunogenetic composition of natural host populations, providing a striking example that the microbial environment shapes the evolution of the host's immune system in the wild.