Digest: Local adaptation at close quarters*

Although the theory of how gene flow and genetic drift interact with local adaptation is well understood, few empirical studies have examined this process. Hämälä et al. (2018) present evidence that adaptive divergence between populations of Arabidopsis lyrata can persist in the face of relatively high levels of gene flow and drift. Maintaining divergence despite gene flow and drift has important implications for understanding adaptive responses of populations in response to human‐driven environmental change.     

Lineage‐specific adaptation to climate involves flowering time in North American Arabidopsis lyrata

Adaptation to local climatic conditions is commonly found within species, but whether it involves the same intraspecific genomic variants is unknown. We studied this question in North American Arabidopsis lyrata, whose current distribution is shaped by post‐glacial range expansion from two refugia, resulting in two distinct genetic clusters covering comparable climatic gradients. Using pooled whole‐genome sequence data of 41 outcrossing populations, we identified loci associated with three niche‐determining climatic variables in the two clusters and compared these outliers. Little evidence was found for parallelism in climate adaptation for single nucleotide polymorphisms (SNPs) and for genes with an accumulation of outlier SNPs. Significantly increased selection coefficients supported them as candidates of climate adaptation. However, the fraction of gene ontology (GO) terms shared between clusters was higher compared to outlier SNPs and outlier genes, suggesting that selection acts on similar pathways but not necessarily the same genes. Enriched GO terms involved responses to abiotic and biotic stress, circadian rhythm and development, with flower development and reproduction being among the most frequently detected. In line with GO enrichment, regulators of flowering time were detected as outlier genes. Our results suggest that while adaptation to environmental gradients on the genomic level are lineage‐specific in A. lyrata, similar biological processes seem to be involved. Differential loss of standing genetic variation, probably driven by genetic drift, can in part account for the lack of parallel evolution on the genomic level.     

Are habitat fragmentation,local adaptation and isolation‐by‐distance driving population divergence in wild rice Oryza rufipogon?

Habitat fragmentation weakens the connection between populations and is accompanied with isolation by distance (IBD) and local adaptation (isolation by adaptation, IBA), both leading to genetic divergence between populations. To understand the evolutionary potential of a population and to formulate proper conservation strategies, information on the roles of IBD and IBA in driving population divergence is critical. The putative ancestor of Asian cultivated rice (Oryza sativa) is endangered in China due to habitat loss and fragmentation. We investigated the genetic variation in 11 Chinese Oryza rufipogon populations using 79 microsatellite loci to infer the effects of habitat fragmentation, IBD and IBA on genetic structure. Historical and current gene flows were found to be rare (m_h = 0.0002–0.0013, m_c = 0.007–0.029), indicating IBD and resulting in a high level of population divergence (F_ST = 0.343). High within‐population genetic variation (H_E = 0.377–0.515), relatively large effective population sizes (N_e = 96–158), absence of bottlenecks and limited gene flow were found, demonstrating little impact of recent habitat fragmentation on these populations. Eleven gene‐linked microsatellite loci were identified as outliers, indicating local adaptation. Hierarchical AMOVA and partial Mantel tests indicated that population divergence of Chinese O. rufipogon was significantly correlated with environmental factors, especially habitat temperature. Common garden trials detected a significant adaptive population divergence associated with latitude. Collectively, these findings imply that IBD due to historical rather than recent fragmentation, followed by local adaptation, has driven population divergence in O. rufipogon.     

Population cytogenetics of <Emphasis Type="Italic">Chironomus circumdatus</Emphasis> Kieffer, 1921 (Diptera,Chironomidae) from Thailand

The objectives of this study were to explore cytogenetic variation and the role of chromosomal change on local adaptation and genetic differentiation of Chironomus circumdatus Kieffer from Thailand. A total of 1,505 larvae from 24 populations were examined cytologically. Twelve chromosomal inversions were found and most of these (9 of 12) were rare inversions. All populations were in Hardy–Weinberg equilibrium. Significant association (P < 0.001) between the A2 and B5 inversions was detected in one population. Population genetic structure analysis indicated significant genetic differentiation between populations (F _ST = 0.037, P < 0.001). Geographic distance was the principal factor limiting gene flow between populations. Nei’s modified genetic distance (D _A) between populations ranged from 0.001 to 0.011 with an average of 0.003. An UPGMA population phenogram depicting relationship between populations based on D _A values revealed three groups of populations, group I, II and III each characterized by different inversions/inversion frequencies. Significant correlation of inversion C3 and water temperature suggested that this inversion might have a role to play on adaptation to high temperature habitat. However, if detection of significant population subdivision and relationship between genetic and geographic distance are taken into account, relationship between C3 and water temperature will also be due to the effect of migration/drift alone without the effect of selection.     

Local selection modifies phenotypic divergence among Rana temporaria populations in the presence of gene flow

In ectotherms, variation in life history traits among populations is common and suggests local adaptation. However, geographic variation itself is not a proof for local adaptation, as genetic drift and gene flow may also shape patterns of quantitative variation. We studied local and regional variation in means and phenotypic plasticity of larval life history traits in the common frog Rana temporaria using six populations from central Sweden, breeding in either open‐canopy or partially closed‐canopy ponds. To separate local adaptation from genetic drift, we compared differentiation in quantitative genetic traits (Q_ST) obtained from a common garden experiment with differentiation in presumably neutral microsatellite markers (F_ST). We found that R. temporaria populations differ in means and plasticities of life history traits in different temperatures at local, and in F_ST at regional scale. Comparisons of differentiation in quantitative traits and in molecular markers suggested that natural selection was responsible for the divergence in growth and development rates as well as in temperature‐induced plasticity, indicating local adaptation. However, at low temperature, the role of genetic drift could not be separated from selection. Phenotypes were correlated with forest canopy closure, but not with geographical or genetic distance. These results indicate that local adaptation can evolve in the presence of ongoing gene flow among the populations, and that natural selection is strong in this system.     

The evolutionary consequences of habitat fragmentation: Body morphology and coloration differentiation among brook trout populations of varying size

A reduction in population size due to habitat fragmentation can alter the relative roles of different evolutionary mechanisms in phenotypic trait differentiation. While deterministic (selection) and stochastic (genetic drift) mechanisms are expected to affect trait evolution, genetic drift may be more important than selection in small populations. We examined relationships between mature adult traits and ecological (abiotic and biotic) variables among 14 populations of brook trout. These naturally fragmented populations have shared ancestry but currently exhibit considerable variability in habitat characteristics and population size (49 < N_c < 10,032; 3 < N_b < 567). Body size, shape, and coloration differed among populations, with a tendency for more variation among small populations in both trait means and CV when compared to large populations. Phenotypic differences were more frequently and directly linked to habitat variation or operational sex ratio than to population size, suggesting that selection may overcome genetic drift at small population size. Phenotype–environment associations were also stronger in females than males, suggesting that natural selection due to abiotic conditions may act more strongly on females than males. Our results suggest that natural and sexual‐selective pressures on phenotypic traits change during the process of habitat fragmentation, and that these changes are largely contingent upon existing habitat conditions within isolated fragments. Our study provides an improved understanding of the ecological and evolutionary consequences of habitat fragmentation and lends insight into the ability of some small populations to respond to selection and environmental change.     

Elevation as a barrier: genetic structure for an Atlantic rain forest tree (Bathysa australis) in the Serra do Mar mountain range,SE Brazil

Distance and discrete geographic barriers play a role in isolating populations, as seed and pollen dispersal become limited. Nearby populations without any geographic barrier between them may also suffer from ecological isolation driven by habitat heterogeneity, which may promote divergence by local adaptation and drift. Likewise, elevation gradients may influence the genetic structure and diversity of populations, particularly those marginally distributed. Bathysa australis (Rubiaceae) is a widespread tree along the elevation gradient of the Serra do Mar, SE Brazil. This self‐compatible species is pollinated by bees and wasps and has autochoric seeds, suggesting restricted gene dispersal. We investigated the distribution of genetic diversity in six B. australis populations at two extreme sites along an elevation gradient: a lowland site (80–216 m) and an upland site (1010–1100 m.a.s.l.). Nine microsatellite loci were used to test for genetic structure and to verify differences in genetic diversity between sites. We found a marked genetic structure on a scale as small as 6 km (F_ST = 0.21), and two distinct clusters were identified, each corresponding to a site. Although B. australis is continuously distributed along the elevation gradient, we have not observed a gene flow between the extreme populations. This might be related to B. australis biological features and creates a potential scenario for adaptation to the different conditions imposed by the elevation gradient. We failed to find an isolation‐by‐distance pattern; although on the fine scale, all populations showed spatial autocorrelation until ~10‐20 m. Elevation difference was a relevant factor though, but we need further sampling effort to check its correlation with genetic distance. The lowland populations had a higher allelic richness and showed higher rare allele counts than the upland ones. The upland site may be more selective, eliminating rare alleles, as we did not find any evidence for bottleneck.     

Local adaptation at range edges: comparing elevation and latitudinal gradients

Local adaptation at range edges influences species’ distributions and how they respond to environmental change. However, the factors that affect adaptation, including gene flow and local selection pressures, are likely to vary across different types of range edge. We performed a reciprocal transplant experiment to investigate local adaptation in populations of Plantago lanceolata and P. major from central locations in their European range and from their latitudinal and elevation range edges (in northern Scandinavia and Swiss Alps, respectively). We also characterized patterns of genetic diversity and differentiation in populations using molecular markers. Range‐centre plants of P. major were adapted to conditions at the range centre, but performed similarly to range‐edge plants when grown at the range edges. There was no evidence for local adaptation when comparing central and edge populations of P. lanceolata. However, plants of both species from high elevation were locally adapted when compared with plants from high latitude, although the reverse was not true. This asymmetry was associated with greater genetic diversity and less genetic differentiation over the elevation gradient than over the latitudinal gradient. Our results suggest that adaptation in some range‐edge populations could increase their performance following climate change. However, responses are likely to differ along elevation and latitudinal gradients, with adaptation more likely at high‐elevation. Furthermore, based upon these results, we suggest that gene flow is unlikely to constrain adaptation in range‐edge populations of these species.     

LOCAL ADAPTATION,PHENOTYPIC DIFFERENTIATION,AND HYBRID FITNESS IN DIVERGED NATURAL POPULATIONS OF ARABIDOPSIS LYRATA

Selection for local adaptation results in genetic differentiation in ecologically important traits. In a perennial, outcrossing model plant Arabidopsis lyrata, several differentiated phenotypic traits contribute to local adaptation, as demonstrated by fitness advantage of the local population at each site in reciprocal transplant experiments. Here we compared fitness components, hierarchical total fitness and differentiation in putatively ecologically important traits of plants from two diverged parental populations from different continents in the native climate conditions of the populations in Norway and in North Carolina (NC, U.S.A.). Survival and number of fruits per inflorescence indicated local advantage at both sites and aster life‐history models provided additional evidence for local adaptation also at the level of hierarchical total fitness. Populations were also differentiated in flowering start date and floral display. We also included reciprocal experimental F₁ and F₂ hybrids to examine the genetic basis of adaptation. Surprisingly, the F₂ hybrids showed heterosis at the study site in Norway, likely because of a combination of beneficial dominance effects from different traits. At the NC site, hybrid fitness was mostly intermediate relative to the parental populations. Local cytoplasmic origin was associated with higher fitness, indicating that cytoplasmic genomes also may contribute to the evolution of local adaptation.     

Water availability drives signatures of local adaptation in whitebark pine (Pinus albicaulis Engelm.) across fine spatial scales of the Lake Tahoe Basin,USA

Patterns of local adaptation at fine spatial scales are central to understanding how evolution proceeds, and are essential to the effective management of economically and ecologically important forest tree species. Here, we employ single and multilocus analyses of genetic data (n = 116 231 SNPs) to describe signatures of fine‐scale adaptation within eight whitebark pine (Pinus albicaulis Engelm.) populations across the local extent of the environmentally heterogeneous Lake Tahoe Basin, USA. We show that despite highly shared genetic variation (F_ST = 0.0069), there is strong evidence for adaptation to the rain shadow experienced across the eastern Sierra Nevada. Specifically, we build upon evidence from a common garden study and find that allele frequencies of loci associated with four phenotypes (mean = 236 SNPs), 18 environmental variables (mean = 99 SNPs), and those detected through genetic differentiation (n = 110 SNPs) exhibit significantly higher signals of selection (covariance of allele frequencies) than could be expected to arise, given the data. We also provide evidence that this covariance tracks environmental measures related to soil water availability through subtle allele frequency shifts across populations. Our results replicate empirical support for theoretical expectations of local adaptation for populations exhibiting strong gene flow and high selective pressures and suggest that ongoing adaptation of many P. albicaulis populations within the Lake Tahoe Basin will not be constrained by the lack of genetic variation. Even so, some populations exhibit low levels of heritability for the traits presumed to be related to fitness. These instances could be used to prioritize management to maintain adaptive potential. Overall, we suggest that established practices regarding whitebark pine conservation be maintained, with the additional context of fine‐scale adaptation.     

Adaptation to reef habitats through selection on the coral animal and its associated microbiome

Spatially adjacent habitats on coral reefs can represent highly distinct environments, often harbouring different coral communities. Yet, certain coral species thrive across divergent environments. It is unknown whether the forces of selection are sufficiently strong to overcome the counteracting effects of the typically high gene flow over short distances, and for local adaptation to occur. We screened the coral genome (using restriction site‐associated sequencing) and characterized both the dinoflagellate photosymbiont‐ and tissue‐associated prokaryote microbiomes (using metabarcoding) of a reef flat and slope population of the reef‐building coral, Pocillopora damicornis, at two locations on Heron Island in the southern Great Barrier Reef. Reef flat and slope populations were separated by <100 m horizontally and ~5 m vertically, and the two study locations were separated by ~1 km. For the coral host, genetic divergence between habitats was much greater than between locations, suggesting limited gene flow between the flat and slope populations. Consistent with environmental selection, outlier loci primarily belonged to the conserved, minimal cellular stress response, likely reflecting adaptation to the different temperature and irradiance regimes on the reef flat and slope. The prokaryote community differed across both habitat and, to a lesser extent, location, whereas the dinoflagellate photosymbionts differed by habitat but not location. The observed intraspecific diversity associated with divergent habitats supports that environmental adaptation involves multiple members of the coral holobiont. Adaptive alleles or microbial associations present in coral populations from the environmentally variable reef flat may provide a source of adaptive variation for assisted evolution approaches, through assisted gene flow, artificial cross‐breeding or probiotic inoculations, with the aim to increase climate resilience in the slope populations.     

Measuring microbial fitness in a field reciprocal transplant experiment

Microbial fitness is easy to measure in the laboratory, but difficult to measure in the field. Laboratory fitness assays make use of controlled conditions and genetically modified organisms, neither of which are available in the field. Among other applications, fitness assays can help researchers detect adaptation to different habitats or locations. We designed a competitive fitness assay to detect adaptation of Saccharomyces paradoxus isolates to the habitat they were isolated from (oak or larch leaf litter). The assay accurately measures relative fitness by tracking genotype frequency changes in the field using digital droplet PCR (DDPCR). We expected locally adapted S. paradoxus strains to increase in frequency over time when growing on the leaf litter type from which they were isolated. The DDPCR assay successfully detected fitness differences among S. paradoxus strains, but did not find a tendency for strains to be adapted to the habitat they were isolated from. Instead, we found that the natural alleles of the hexose transport gene we used to distinguish S. paradoxus strains had significant effects on fitness. The origin of a strain also affected its fitness: strains isolated from oak litter were generally fitter than strains from larch litter. Our results suggest that dispersal limitation and genetic drift shape S. paradoxus populations in the forest more than local selection does, although further research is needed to confirm this. Tracking genotype frequency changes using DDPCR is a practical and accurate microbial fitness assay for natural environments.     

Impact of demography on linked selection in two outcrossing Brassicaceae species

Genetic diversity is shaped by mutation, genetic drift, gene flow, recombination, and selection. The dynamics and interactions of these forces shape genetic diversity across different parts of the genome, between populations and species. Here, we have studied the effects of linked selection on nucleotide diversity in outcrossing populations of two Brassicaceae species, Arabidopsis lyrata and Capsella grandiflora, with contrasting demographic history. In agreement with previous estimates, we found evidence for a modest population size expansion thousands of generations ago, as well as efficient purifying selection in C. grandiflora. In contrast, the A. lyrata population exhibited evidence for very recent strong population size decline and weaker efficacy of purifying selection. Using multiple regression analyses with recombination rate and other genomic covariates as explanatory variables, we can explain 47% of the variance in neutral diversity in the C. grandiflora population, while in the A. lyrata population, only 11% of the variance was explained by the model. Recombination rate had a significant positive effect on neutral diversity in both species, suggesting that selection at linked sites has an effect on patterns of neutral variation. In line with this finding, we also found reduced neutral diversity in the vicinity of genes in the C. grandiflora population. However, in A. lyrata no such reduction in diversity was evident, a finding that is consistent with expectations of the impact of a recent bottleneck on patterns of neutral diversity near genes. This study thus empirically demonstrates how differences in demographic history modulate the impact of selection at linked sites in natural populations.     

Population genetics and fitness in fragmented populations of the dioecious and endangered <Emphasis Type="Italic">Silene otites</Emphasis> (Caryophyllaceae)

Population fragmentation is often correlated with loss of genetic diversity and reduced fitness. Obligate out-crossing (dioecy) is expected to enhance genetic diversity, reduce genetic differentiation, and avoid inbreeding depression through frequent gene flow. However, in highly fragmented populations dioecy has only diminishing effects upon genetic structure as pollination limitations (e.g. flight distance of pollinators) most often restrict inter-population gene flow in insect pollinated species. In fragmented dry grasslands in northeastern Germany, we analysed genetic structure, fitness, and habitat quality of the endangered dioecious Silene otites (Caryophyllaceae). Using AFLP markers, a high level of differentiation among ten populations was found (F _st = 0.36), while the intra-population genetic diversities (H _E = 0.165–0.240) were similar as compared to hermaphroditic species. There was neither a correlation between geographic and genetic distance nor between genetic diversity and population size, which indicates reduced gene flow among populations and random genetic drift. Plant size was positively correlated with genetic diversity. Seed set and number of juveniles were positively related to population size. Higher total coverage resulted in reduced plant fitness, and the number of juveniles was negatively correlated to cryptogam cover. Additionally, we found a sex ratio bias towards more male plants in larger populations. Overall, our results indicate that on a regional geographic scale dioecy does not necessarily prevent genetic erosion in the case of habitat fragmentation, especially in the absence of long distance seed and pollen dispersal capacity.     

Drift happens: Molecular genetic diversity and differentiation among populations of jewelweed (Impatiens capensis Meerb.) reflect fragmentation of floodplain forests

Landscape features often shape patterns of gene flow and genetic differentiation in plant species. Populations that are small and isolated enough also become subject to genetic drift. We examined patterns of gene flow and differentiation among 12 floodplain populations of the selfing annual jewelweed (Impatiens capensis Meerb.) nested within four river systems and two major watersheds in Wisconsin, USA. Floodplain forests and marshes provide a model system for assessing the effects of habitat fragmentation within agricultural/urban landscapes and for testing whether rivers act to genetically connect dispersed populations. We generated a panel of 12,856 single nucleotide polymorphisms and assessed genetic diversity, differentiation, gene flow, and drift. Clustering methods revealed strong population genetic structure with limited admixture and highly differentiated populations (mean multilocus F_ST = 0.32, F_ST’ = 0.33). No signals of isolation by geographic distance or environment emerged, but alleles may flow along rivers given that genetic differentiation increased with river distance. Differentiation also increased in populations with fewer private alleles (R² = 0.51) and higher local inbreeding (R² = 0.22). Populations varied greatly in levels of local inbreeding (F_IS = 0.2–0.9) and F_IS increased in more isolated populations. These results suggest that genetic drift dominates other forces in structuring these Impatiens populations. In rapidly changing environments, species must migrate or genetically adapt. Habitat fragmentation limits both processes, potentially compromising the ability of species to persist in fragmented landscapes.     

Long‐term ‘islands’ in the landscape: low gene flow,effective population size and genetic divergence in the shrub Hakea oldfieldii (Proteaceae)

The genetic structure of disjunct populations is determined by founding genetic properties, demographic processes, gene flow, drift and local selection. We aim to identify the genetic consequences of natural population disjunction at regional and local scales in Hakea oldfieldii using nuclear and plastid markers to investigate long‐term effective population sizes and gene flow, and patterns of diversity and divergence, among populations. Regional divergence was significant as shown by a consistent pattern in principal coordinates, neighbor‐joining and Bayesian analyses, but divergence at the local level was also significant with localized distribution of plastid haplotypes and populations clustering separately in Bayesian analyses. Historical, recent and first‐generation gene flow was low, suggesting that recent habitat fragmentation has not reduced gene migration significantly. Genetic bottlenecks were detected in three populations. Long‐term effective population size was significantly correlated with the number of alleles/locus and observed heterozygosity, but not with census population size, suggesting that the loss of diversity is associated with long‐term changes rather than recent fragmentation. Inbreeding coefficients were significant in only three populations, suggesting that the loss of diversity is linked to drift and bottlenecks associated with demographic processes (local extinction by fires) rather than inbreeding. Historical disjunction as a result of specific ecological requirements, contraction of habitats following drying during the Pleistocene, low gene flow and changes in population size are likely to have been important forces driving divergence through isolation by distance and drift. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 319–334.     

Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction‐site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small N_e (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome‐wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high F_ST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high F_ST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small N_e in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.     

Exogenous selection rather than cytonuclear incompatibilities shapes asymmetrical fitness of reciprocal Arabidopsis hybrids

Reciprocal crosses between species often display an asymmetry in the fitness of F₁ hybrids. This pattern, referred to as isolation asymmetry or Darwin's corollary to Haldane's rule, is a general feature of reproductive isolation in plants, yet factors determining its magnitude and direction remain unclear. We evaluated reciprocal species crosses between two naturally hybridizing diploid species of Arabidopsis to assess the degree of isolation asymmetry at different postmating life stages. We found that pollen from Arabidopsis arenosa will usually fertilize ovules from Arabidopsis lyrata; the reverse receptivity being less complete. Maternal A. lyrata parents set more F₁ hybrid seed, but germinate at lower frequency, reversing the asymmetry. As predicted by theory, A. lyrata (the maternal parent with lower seed viability in crosses) exhibited accelerated chloroplast evolution, indicating that cytonuclear incompatibilities may play a role in reproductive isolation. However, this direction of asymmetrical reproductive isolation is not replicated in natural suture zones, where delayed hybrid breakdown of fertility at later developmental stages, or later‐acting selection against A. arenosa maternal hybrids (unrelated to hybrid fertility, e.g., substrate adaptation) may be responsible for an excess of A. lyrata maternal hybrids. Exogenous selection rather than cytonuclear incompatibilities thus shapes the asymmetrical postmating isolation in nature.