The degree of adaptive phenotypic plasticity is correlated with the spatial environmental heterogeneity experienced by island populations of Rana temporaria

Although theoretical models have identified environmental heterogeneity as a prerequisite for the evolution of adaptive plasticity, this relationship has not yet been demonstrated experimentally. Because of pool desiccation risk, adaptation of development rate is important for many amphibians. In a simulated pool-drying experiment, we compared the development time and phenotypic plasticity in development time of populations of the common frog Rana temporaria, originating from 14 neighbouring islands off the coast of northern Sweden. Drying regime of pools used by frogs for breeding differed within and among the islands. We found that the degree of phenotypic plasticity in development time was positively correlated with the spatial variation in the pool-drying regimes present on each island. In addition, local adaptation in development time to the mean drying rate of the pools on each island was found. Hence, our study demonstrates the connection between environmental heterogeneity and developmental plasticity at the island population level, and also highlights the importance of the interplay between local specialization and phenotypic plasticity depending on the local selection pressures.     

Spatial variation in climate mediates gene flow across an island archipelago

High levels of gene flow among partially isolated populations can overwhelm selection and limit local adaptation. This process, known as “gene swamping,” can homogenize genetic diversity among populations and reduce the capacity of a species to withstand rapid environmental change. We studied brown anole lizards (Anolis sagrei) distributed across seven islands in The Bahamas. We used microsatellite markers to estimate gene flow among islands and then examined the correlation between thermal performance and island temperature. The thermal optimum for sprint performance was correlated with both mean and maximum island temperature, whereas performance breadth was not correlated with any measure of temperature variation. Gene flow between islands decreased as the difference between mean island temperatures increased, even when those islands were adjacent to one another. These data suggest that phenotypic variation is the result of either (1) local genetic adaptation with selection against immigrants maintaining variation in the thermal optimum, (2) irreversible forms of adaptive plasticity such that immigrants have reduced fitness, or (3) an interaction between fixed genetic differences and plasticity. In general, the patterns of gene flow we observed suggest that local thermal environments represent important ecological filters that can mediate gene flow on relatively fine geographic scales.     

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.     

Local adaptation with high gene flow: temperature parameters drive adaptation to altitude in the common frog (Rana temporaria)

Both environmental and genetic influences can result in phenotypic variation. Quantifying the relative contributions of local adaptation and phenotypic plasticity to phenotypes is key to understanding the effect of environmental variation on populations. Identifying the selective pressures that drive divergence is an important, but often lacking, next step. High gene flow between high‐ and low‐altitude common frog (Rana temporaria) breeding sites has previously been demonstrated in Scotland. The aim of this study was to assess whether local adaptation occurs in the face of high gene flow and to identify potential environmental selection pressures that drive adaptation. Phenotypic variation in larval traits was quantified in R. temporaria from paired high‐ and low‐altitude sites using three common temperature treatments. Local adaptation was assessed using Q_ST–F_ST analyses, and quantitative phenotypic divergence was related to environmental parameters using Mantel tests. Although evidence of local adaptation was found for all traits measured, only variation in larval period and growth rate was consistent with adaptation to altitude. Moreover, this was only evident in the three mountains with the highest high‐altitude sites. This variation was correlated with mean summer and winter temperatures, suggesting that temperature parameters are potentially strong selective pressures maintaining local adaptation, despite high gene flow.     

Genomic islands of divergence linked to ecotypic variation in sockeye salmon

Regions of the genome displaying elevated differentiation (genomic islands of divergence) are thought to play an important role in local adaptation, especially in populations experiencing high gene flow. However, the characteristics of these islands as well as the functional significance of genes located within them remain largely unknown. Here, we used data from thousands of SNPs aligned to a linkage map to investigate genomic islands of divergence in three ecotypes of sockeye salmon (Oncorhynchus nerka) from a single drainage in southwestern Alaska. We found ten islands displaying high differentiation among ecotypes. Conversely, neutral structure observed throughout the rest of the genome was low and not partitioned by ecotype. One island on linkage group So13 was particularly large and contained six SNPs with F_ST > 0.14 (average F_ST of neutral SNPs = 0.01). Functional annotation revealed that the peak of this island contained a nonsynonymous mutation in a gene involved in growth in other species (TULP4). The islands that we discovered were relatively small (80–402 Kb), loci found in islands did not show reduced levels of diversity, and loci in islands displayed slightly elevated linkage disequilibrium. These attributes suggest that the islands discovered here were likely generated by divergence hitchhiking; however, we cannot rule out the possibility that other mechanisms may have produced them. Our results suggest that islands of divergence serve an important role in local adaptation with gene flow and represent a significant advance towards understanding the genetic basis of ecotypic differentiation.     

Geographic variation in phenotypic plasticity in response to dissolved oxygen in an African cichlid fish

Genetic adaptation and phenotypic plasticity are two ways in which organisms can adapt to local environmental conditions. We examined genetic and plastic variation in gill and brain size among swamp (low oxygen; hypoxic) and river (normal oxygen; normoxic) populations of an African cichlid fish, Pseudocrenilabrus multicolor victoriae. Larger gills and smaller brains should be advantageous when oxygen is low, and we hypothesized that the relative contribution of local genetic adaptation vs. phenotypic plasticity should be related to potential for dispersal between environments (because of gene flow’s constraint on local genetic adaptation). We conducted a laboratory‐rearing experiment, with broods from multiple populations raised under high‐oxygen and low‐oxygen conditions. We found that most of the variation in gill size was because of plasticity. However, both plastic and genetic effects on brain mass were detected, as were genetic effects on brain mass plasticity. F₁ offspring from populations with the highest potential for dispersal between environments had characteristically smaller and more plastic brains. This phenotypic pattern might be adaptive in the face of gene flow, if smaller brains and increased plasticity confer higher average fitness across environment types.     

Microgeographic adaptations of spotted salamander morphological defenses in response to a predaceous salamander and beetle

Spatial heterogeneity in the selection imposed by different predator species could promote the adaptive diversification of local prey populations. However, high gene flow might swamp local adaptations at limited spatial scales or generalized phenotypic plasticity might evolve in place of local diversification. Spotted salamander larvae Ambystoma maculatum face strongly varying risks from gape‐limited marbled salamander larvae Ambystoma opacum and gape‐unconstrained diving beetle larvae Dytiscus spp. across natural landscapes. To evaluate if A. maculatum adapts to these predation risk across micro‐geographic scales, I measured selection gradients in response to the two focal predators and then assayed the defensive morphologies of ten populations in a common garden experiment. I found that A. opacum induced selection on A. maculatum for larger tailfins and bodies whereas beetles induced selection for larger tail muscles and smaller bodies. In accordance with the local adaptation hypothesis, A. maculatum populations inhabiting ponds with high beetle densities grew larger tail muscles relative to other populations when raised in a common environment. However, populations exposed to strong A. opacum selection did not evolve larger tailfins as predicted. High gene flow or morphological plasticity could explain the absence of this morphological response to A. opacum. Overall, results suggest that populations can sometimes evolve adaptive traits in response to locally variable selection regimes even across the very limited distances that separate populations in this study. If prey populations often differ in their defenses against local predators, then this variation could affect the outcome of species interactions in local communities.     

Role of selection and gene flow in population differentiation at the edge vs. interior of the species range differing in climatic conditions

Evaluating the relative importance of neutral and adaptive processes as determinants of population differentiation across environments is a central theme of evolutionary biology. We applied the Q_ST–F_ST comparison flanked by a direct test for local adaptation to infer the role of climate‐driven selection and gene flow in population differentiation of an annual grass Avena sterilis in two distinct parts of the species range, edge and interior, which represent two globally different climates, desert and Mediterranean. In a multiyear reciprocal transplant experiment, the plants of desert and Mediterranean origin demonstrated home advantage, and population differentiation in several phenotypic traits related to reproduction exceeded neutral predictions, as determined by comparisons of Q_ST values with theoretical F_ST distributions. Thus, variation in these traits likely resulted from local adaptation to desert and Mediterranean environments. The two separate common garden experiments conducted with different experimental design revealed that two population comparisons, in contrast to multi‐population comparisons, are likely to detect population differences in virtually every trait, but many of these differences reflect effects of local rather than regional environment. We detected a general reduction in neutral (SSR) genetic variation but not in adaptive quantitative trait variation in peripheral desert as compared with Mediterranean core populations. On the other hand, the molecular data indicated intensive gene flow from the Mediterranean core towards desert periphery. Although species range position in our study (edge vs. interior) was confounded with climate (desert vs. Mediterranean), the results suggest that the gene flow from the species core does not have negative consequences for either performance of the peripheral plants or their adaptive potential.     

Adaptive divergence in body size overrides the effects of plasticity across natural habitats in the brown trout

The evolution of life-history traits is characterized by trade-offs between different selection pressures, as well as plasticity across environmental conditions. Yet, studies on local adaptation are often performed under artificial conditions, leaving two issues unexplored: (i) how consistent are laboratory inferred local adaptations under natural conditions and (ii) how much phenotypic variation is attributed to phenotypic plasticity and to adaptive evolution, respectively, across environmental conditions? We reared fish from six locally adapted (domesticated and wild) populations of anadromous brown trout (Salmo trutta) in one semi-natural and three natural streams and recorded a key life-history trait (body size at the end of first growth season). We found that population-specific reaction norms were close to parallel across different streams and Q_ST was similar – and larger than F_ST – within all streams, indicating a consistency of local adaptation in body size across natural environments. The amount of variation explained by population origin exceeded the variation across stream environments, indicating that genetic effects derived from adaptive processes have a stronger effect on phenotypic variation than plasticity induced by environmental conditions. These results suggest that plasticity does not “swamp” the phenotypic variation, and that selection may thus be efficient in generating genetic change.     

The role of selection and historical factors in driving population differentiation along an elevational gradient in an island bird

Adaptation to local environmental conditions and the range dynamics of populations can influence evolutionary divergence along environmental gradients. Thus, it is important to investigate patterns of both phenotypic and genetic variations among populations to reveal the respective roles of these two types of factors in driving population differentiation. Here, we test for evidence of phenotypic and genetic structure across populations of a passerine bird (Zosterops borbonicus) distributed along a steep elevational gradient on the island of Réunion. Using 11 microsatellite loci screened in 401 individuals from 18 localities distributed along the gradient, we found that genetic differentiation occurred at two spatial levels: (i) between two main population groups corresponding to highland and lowland areas, respectively, and (ii) within each of these two groups. In contrast, several morphological traits varied gradually along the gradient. Comparison of neutral genetic differentiation (F_ST) and phenotypic differentiation (P_ST) showed that P_ST largely exceeds F_ST at several morphological traits, which is consistent with a role for local adaptation in driving morphological divergence along the gradient. Overall, our results revealed an area of secondary contact midway up the gradient between two major, cryptic, population groups likely diverged in allopatry. Remarkably, local adaptation has shaped phenotypic differentiation irrespective of population history, resulting in different patterns of variation along the elevational gradient. Our findings underscore the importance of understanding both historical and selective factors when trying to explain variation along environmental gradients.     

Detection of environmental and morphological adaptation despite high landscape genetic connectivity in a pest grasshopper (Phaulacridium vittatum)

Widespread species that exhibit both high gene flow and the capacity to occupy heterogeneous environments make excellent models for examining local selection processes along environmental gradients. Here we evaluate the influence of temperature and landscape variables on genetic connectivity and signatures of local adaptation in Phaulacridium vittatum, a widespread agricultural pest grasshopper, endemic to Australia. With sampling across a 900‐km latitudinal gradient, we genotyped 185 P. vittatum from 19 sites at 11,408 single nucleotide polymorphisms (SNPs) using ddRAD sequencing. Despite high gene flow across sites (pairwise F_ST = 0.0003–0.08), landscape genetic resistance modelling identified a positive nonlinear effect of mean annual temperature on genetic connectivity. Urban areas and water bodies had a greater influence on genetic distance among sites than pasture, agricultural areas and forest. Together, F_ST outlier tests and environmental association analysis (EAA) detected 242 unique SNPs under putative selection, with the highest numbers associated with latitude, mean annual temperature and body size. A combination of landscape genetic connectivity analysis together with EAA identified mean annual temperature as a key driver of both neutral gene flow and environmental selection processes. Gene annotation of putatively adaptive SNPs matched with gene functions for olfaction, metabolic detoxification and ultraviolet light shielding. Our results imply that this widespread agricultural pest has the potential to spread and adapt under shifting temperature regimes and land cover change.     

Evolution of the G-matrix in life history traits in the common frog during a recent colonisation of an island system

Studies of genetic correlations between traits that ostensibly channel the path of evolution away from the direction of natural selection require information on key aspects such as ancestral phenotypes, the duration of adaptive evolution, the direction of natural selection, and genetic covariances. In this study we provide such information in a frog population system. We studied adaptation in life history traits to pool drying in frog populations on islands of known age, which have been colonized from a mainland population. The island populations show strong local adaptation in development time and size. We found that the first eigenvector of the variance–covariance matrix (g _max) had changed between ancestral mainland populations and newly established island populations. Interestingly, there was no divergence in g _max among island populations that differed in their local adaptation in development time and size. Thus, a major change in the genetic covariance of life-history traits occurred in the colonization of the island system, but subsequent local adaptation in development time took place despite the constraints imposed by the genetic covariance structure.     

Isolation by distance,not incipient ecological speciation,explains genetic differentiation in an Andean songbird (Aves: Furnariidae: Cranioleuca antisiensis,Line‐cheeked Spinetail) despite near threefold body size change across an environmental gradient

During the process of ecological speciation, reproductive isolation results from divergent natural selection and leads to a positive correlation between genetic divergence and adaptive phenotypic divergence, that is, isolation by adaptation (IBA). In natural populations, phenotypic differentiation is often autocorrelated with geographic distance, making IBA difficult to distinguish from the neutral expectation of isolation by distance (IBD). We examined these two alternatives in a dramatic case of clinal phenotypic variation in an Andean songbird, the Line‐cheeked Spinetail (Cranioleuca antisiensis). At its geographic extremes, this species shows a near threefold difference in body mass (11.5 to 31.0 g) with marked plumage differences. We analysed phenotypic, environmental and genetic data (5,154 SNPs) from 172 individuals and 19 populations sampled along its linear distribution in the Andes. We found that body mass was tightly correlated with environmental temperature, consistent with local adaptation as per Bergmann's rule. Using a P_ST–F_ST analysis, we found additional support for natural selection driving body mass differentiation, but these results could also be explained by environment‐mediated phenotypic plasticity. When we assessed the relative support for patterns of IBA and IBD using variance partitioning, we found that IBD was the best explanation for genetic differentiation along the cline. Adaptive phenotypic or environmental divergence can reduce gene flow, a pattern interpreted as evidence of ecological speciation's role in diversification. Our results provide a counterexample to this interpretation. Despite conditions conducive to ecological speciation, our results suggest that dramatic size and environmental differentiation within C. antisiensis are not limiting gene flow.     

Rolling stones and stable homes: social structure,habitat diversity and population genetics of the Hawaiian spinner dolphin (Stenella longirostris)

Spinner dolphins (Stenella longirostris) exhibit different social behaviours at two regions in the Hawaiian Archipelago: off the high volcanic islands in the SE archipelago they form dynamic groups with ever‐changing membership, but in the low carbonate atolls in the NW archipelago they form long‐term stable groups. To determine whether these environmental and social differences influence population genetic structure, we surveyed spinner dolphins throughout the Hawaiian Archipelago with mtDNA control region sequences and 10 microsatellite loci (n = 505). F‐statistics, Bayesian cluster analyses, and assignment tests revealed population genetic separations between most islands, with less genetic structuring among the NW atolls than among the SE high islands. The populations with the most stable social structure (Midway and Kure Atolls) have the highest gene flow between populations (mtDNA Φ_ST < 0.001, P = 0.357; microsatellite F_ST = ?0.001; P = 0.597), and a population with dynamic groups and fluid social structure (the Kona Coast of the island of Hawai’i) has the lowest gene flow (mtDNA 0.042 < Φ_ST < 0.236, P < 0.05; microsatellite 0.016 < F_ST < 0.040, P < 0.001). We suggest that gene flow, dispersal, and social structure are influenced by the availability of habitat and resources at each island. Genetic comparisons to a South Pacific location (n = 16) indicate that Hawaiian populations are genetically depauperate and isolated from other Pacific locations (mtDNA 0.216 < F_ST < 0.643, P < 0.001; microsatellite 0.058 < F_ST < 0.090, P < 0.001); this isolation may also influence social and genetic structure within Hawai’i. Our results illustrate that genetic and social structure are flexible traits that can vary between even closely‐related populations.     

Genetic structure of a reef-building coral from thermally distinct environments on the Great Barrier Reef

Adaptation to localised thermal regimes is facilitated by restricted gene flow, ultimately leading to genetic divergence among populations and differences in their physiological tolerances. Allozyme analysis of six polymorphic loci was used to assess genetic differentiation between nine populations of the reef-building coral Acropora millepora over a latitudinal temperature gradient on the inshore regions of the Great Barrier Reef (GBR). Small but significant genetic differentiation indicative of moderate levels of gene flow (pairwise F _ST 0.023 to 0.077) was found between southern populations of A. millepora in cooler regions of the GBR and the warmer, central or northern GBR populations. Patterns of genetic differentiation at these putatively neutral allozyme loci broadly matched experimental variation in thermal tolerance and were consistent with local thermal regimes (warmest monthly-averages) for the A. millepora populations examined. It is therefore hypothesized that natural selection has influenced the thermal tolerance of the A. millepora populations examined and greater genetic divergence is likely to be revealed by examination of genetic markers under the direct effects of natural selection.     

CORRELATION OF PAIRWISE GENETIC AND GEOGRAPHIC DISTANCE MEASURES: INFERRING THE RELATIVE INFLUENCES OF GENE FLOW AND DRIFT ON THE DISTRIBUTION OF GENETIC VARIABILITY

Attempts to relate estimates of regional F_ST to gene flow and drift via Wright's (1931) equation F_ST ≈ 1/ (4Nm + 1) are often inappropriate because most natural sets of populations probably are not at equilibrium (McCauley 1993), as assumed by the island model upon which the equation is based, or ineffective because the influences of gene flow and drift are confounded in the product Nm. Evaluations of the association between genetic (F_ST) and geographic distances separating all pairwise populations combinations in a region allows one to test for regional equilibrium, to evaluate the relative influences of gene flow and drift on population structure both within and between regions, and to visualize the behavior of the association across all degrees of geographic separation. Tests of the model using microsatellite data from 51 populations of eastern collared lizards (Crotaphytus collaris collaris) collected from four distinct geographical regions gave results highly consistent with predicted patterns of association based on regional differences in various historical and ecological factors that affect the amount of drift and gene flow. The model provides a prerequisite for and an alternative to regional F_ST analyses, which often simply assume regional equilibrium, thus potentially leading to erroneous and misleading inferences regarding regional population structure.     

Parasite‐mediated selection in a natural metapopulation of Daphnia magna

Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, nonadaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a Q_ST–F_ST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.     

Patterns of Genetic Variability in Island Populations of the Cane Toad (Rhinella marina) from the Mouth of the Amazon

The Amazonian coast has several unique geological characteristics resulting from the interaction between drainage pattern of the Amazon River and the Atlantic Ocean. It is one of the most extensive and sedimentologically dynamic regions of the world, with a large number of continental islands mostly formed less than 10,000 years ago. The natural distribution of the cane toad (Rhinella marina), one of the world’s most successful invasive species, in this complex Amazonian system provides an intriguing model for the investigation of the effects of isolation or the combined effects of isolation and habitat dynamic changes on patterns of genetic variability and population differentiation. We used nine fast-evolving microsatellite loci to contrast patterns of genetic variability in six coastal (three mainlands and three islands) populations of the cane toad near the mouth of the Amazon River. Results from Bayesian multilocus clustering approach and Discriminant Analyses of Principal Component were congruent in showing that each island population was genetically differentiated from the mainland populations. All F_ST values obtained from all pairwise comparisons were significant, ranging from 0.048 to 0.186. Estimates of both recent and historical gene flow were not significantly different from zero across all population pairs, except the two mainland populations inhabiting continuous habitats. Patterns of population differentiation, with a high level of population substructure and absence/restricted gene flow, suggested that island populations of R. marina are likely isolated since the Holocene sea-level rise. However, considering the similar levels of genetic variability found in both island and mainland populations, it is reliable to assume that they were also isolated for longer periods. Given the genetic uniqueness of each cane toad population, together with the high natural vulnerability of the coastal regions and intense human pressures, we suggest that these populations should be treated as discrete units for conservation management purposes.