Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration

Local adaptation is a major mechanism underlying the maintenance of phenotypic variation in spatially heterogeneous environments. In the barn owl (Tyto alba), dark and pale reddish-pheomelanic individuals are adapted to conditions prevailing in northern and southern Europe, respectively. Using a long-term dataset from Central Europe, we report results consistent with the hypothesis that the different pheomelanic phenotypes are adapted to specific local conditions in females, but not in males. Compared to whitish females, reddish females bred in sites surrounded by more arable fields and less forests. Colour-dependent habitat choice was apparently beneficial. First, whitish females produced more fledglings when breeding in wooded areas, whereas reddish females when breeding in sites with more arable fields. Second, cross-fostering experiments showed that female nestlings grew wings more rapidly when both their foster and biological mothers were of similar colour. The latter result suggests that mothers should particularly produce daughters in environments that best match their own coloration. Accordingly, whiter females produced fewer daughters in territories with more arable fields. In conclusion, females displaying alternative melanic phenotypes bred in habitats providing them with the highest fitness benefits. Although small in magnitude, matching habitat selection and local adaptation may help maintain variation in pheomelanin coloration in the barn owl.     

Evolution of polygenic traits under global vs local adaptation

Observations about the number, frequency, effect size, and genomic distribution of alleles associated with complex traits must be interpreted in light of evolutionary process. These characteristics, which constitute a trait’s genetic architecture, can dramatically affect evolutionary outcomes in applications from agriculture to medicine, and can provide a window into how evolution works. Here, I review theoretical predictions about the evolution of genetic architecture under spatially homogeneous, global adaptation as compared with spatially heterogeneous, local adaptation. Due to the tension between divergent selection and migration, local adaptation can favor “concentrated” genetic architectures that are enriched for alleles of larger effect, clustered in a smaller number of genomic regions, relative to expectations under global adaptation. However, the evolution of such architectures may be limited by many factors, including the genotypic redundancy of the trait, mutation rate, and temporal variability of environment. I review the circumstances in which predictions differ for global vs local adaptation and discuss where progress can be made in testing hypotheses using data from natural populations and lab experiments. As the field of comparative population genomics expands in scope, differences in architecture among traits and species will provide insights into how evolution works, and such differences must be interpreted in light of which kind of selection has been operating.     

Liking the good guys: amplifying local adaptation via the evolution of condition‐dependent mate choice

Local adaptation can be strengthened through a diversity of mechanisms that reduce gene flow between contrasting environments. Recent work revealed that mate choice could enhance local adaptation when females preferentially mate with locally adapted males and that such female preferences readily evolve, but the opposing effects of recombination, migration and costs of female preferences remain relatively unexplored. To investigate these effects, we develop a two‐patch model with two genes, one influencing an ecological trait and one influencing female preferences, where both male signals and female preferences are allowed to depend on the match between an individual's ecological trait and the local environment (condition). Because trait variation is limited when migration is rare and the benefits of preferential mating are short‐lived when migration is frequent, we find that female preferences for males in high condition spread most rapidly with intermediate levels of migration. Surprisingly, we find that preferences for locally adapted males spread fastest with higher recombination rates, which contrasts with earlier studies. This is because a stronger preference allele for locally adapted males can only get uncoupled from maladapted ecological alleles following migration through recombination. The effects of migration and recombination depend strongly on the condition of the males being chosen by females, but only weakly on the condition of the females doing the choosing, except when it comes to the costs of preference. Although costs always impede the spread of female preferences for locally adapted males, the impact is substantially lessened if costs are borne primarily by females in poor condition. The abundance of empirical examples of condition‐dependent mate choice combined with our theoretical results suggests that the evolution of mate choice could commonly facilitate local adaptation in nature.     

Evolution of the distribution of dispersal distance under distance‐dependent cost of dispersal

Abstract We analyse the evolution of the distribution of dispersal distances in a stable and homogeneous environment in one‐ and two‐dimensional habitats. In this model, dispersal evolves to avoid the competition between relatives although some cost might be associated with this behaviour. The evolutionarily stable dispersal distribution is characterized by an equilibration of the fitness gains among all the different dispersal distances. This cost‐benefit argument has heuristic value and facilitates the comprehension of results obtained numerically. In particular, it explains why some minimal or maximal probability of dispersal may evolve at intermediate distances when the cost of dispersal function is an increasing function of distance. We also show that kin selection may favour long range dispersal even if the survival cost of dispersal is very high, provided the survival probability does not vanish at long distances.     

Fitness declines towards range limits and local adaptation to climate affect dispersal evolution during climate‐induced range shifts

Dispersal ability will largely determine whether species track their climatic niches during climate change, a process especially important for populations at contracting (low‐latitude/low‐elevation) range limits that otherwise risk extinction. We investigate whether dispersal evolution at contracting range limits is facilitated by two processes that potentially enable edge populations to experience and adjust to the effects of climate deterioration before they cause extinction: (i) climate‐induced fitness declines towards range limits and (ii) local adaptation to a shifting climate gradient. We simulate a species distributed continuously along a temperature gradient using a spatially explicit, individual‐based model. We compare range‐wide dispersal evolution during climate stability vs. directional climate change, with uniform fitness vs. fitness that declines towards range limits (RLs), and for a single climate genotype vs. multiple genotypes locally adapted to temperature. During climate stability, dispersal decreased towards RLs when fitness was uniform, but increased when fitness declined towards RLs, due to highly dispersive genotypes maintaining sink populations at RLs, increased kin selection in smaller populations, and an emergent fitness asymmetry that favoured dispersal in low‐quality habitat. However, this initial dispersal advantage at low‐fitness RLs did not facilitate climate tracking, as it was outweighed by an increased probability of extinction. Locally adapted genotypes benefited from staying close to their climate optima; this selected against dispersal under stable climates but for increased dispersal throughout shifting ranges, compared to cases without local adaptation. Dispersal increased at expanding RLs in most scenarios, but only increased at the range centre and contracting RLs given local adaptation to climate.     

Influence of host use adaptation on the dispersal propensity of Callosobruchus maculatus

Local adaptation can lead to significant differences in host use that may influence population growth and spread. Here, we test the potential for adaptation of one behavioural component (host acceptance) to lead to cross‐adaptation for a separate behavioural component (dispersal propensity) using the cowpea seed beetle, Callosobruchus maculatus. C. maculatus originating from the same source population were subjected to selection for host use by rearing them for over 40 generations on either the preferred host of the ancestral population, Vigna radiata, or a marginal host for the ancestral population, Cicer arietinum. Host acceptance was then assayed using four choice and no‐choice oviposition assays including a low‐quality host, Lens culinaris, a marginal host, C. arietinum, and two high‐quality hosts, V. radiata and V. unguiculata. Dispersal was assayed in interconnected arenas containing one of three different hosts: V. radiata, V. unguiculata or C. arietinum. As expected, differences in host acceptance were present, in this case consisting of greater acceptance of the lower quality hosts in the C. arietinum population, but no significant differences in host preference hierarchy. Dispersal propensity in the C. arietinum population was significantly lower than in the V. radiata population, despite the absence of any difference in selection pressures for dispersal. Furthermore, significant differences in dispersal propensity in arenas containing different hosts were present in the V. radiata population, but not in the C. arietinum population. Results highlight the need to consider local adaptation when developing management recommendations, even for behaviours for which selection pressures are not directly apparent.     

After the games are over: life‐history trade‐offs drive dispersal attenuation following range expansion

Increased dispersal propensity often evolves on expanding range edges due to the Olympic Village effect, which involves the fastest and fittest finding themselves together in the same place at the same time, mating, and giving rise to like individuals. But what happens after the range's leading edge has passed and the games are over? Although empirical studies indicate that dispersal propensity attenuates following range expansion, hypotheses about the mechanisms driving this attenuation have not been clearly articulated or tested. Here, we used a simple model of the spatiotemporal dynamics of two phenotypes, one fast and the other slow, to propose that dispersal attenuation beyond preexpansion levels is only possible in the presence of trade‐offs between dispersal and life‐history traits. The Olympic Village effect ensures that fast dispersers preempt locations far from the range's previous limits. When trade‐offs are absent, this preemptive spatial advantage has a lasting impact, with highly dispersive individuals attaining equilibrium frequencies that are strictly higher than their introduction frequencies. When trade‐offs are present, dispersal propensity decays rapidly at all locations. Our model's results about the postcolonization trajectory of dispersal evolution are clear and, in principle, should be observable in field studies. We conclude that empirical observations of postcolonization dispersal attenuation offer a novel way to detect the existence of otherwise elusive trade‐offs between dispersal and life‐history traits.     

Using connectivity to identify climatic drivers of local adaptation: a response to Macdonald et al.

Macdonald et al. (Ecol. Lett., 21, 2018, 207–216) proposed an analytical framework for identifying evolutionary processes underlying trait‐environment relationships observed in natural populations. Here, we propose an expanded and refined framework based on simulations and bootstrap‐based approaches, and we elaborate on an important statistical caveat common to most datasets.     

A meta‐analysis of dispersal in butterflies

Dispersal has recently gained much attention because of its crucial role in the conservation and evolution of species facing major environmental changes such as habitat loss and fragmentation, climate change, and their interactions. Butterflies have long been recognized as ideal model systems for the study of dispersal and a huge amount of data on their ability to disperse has been collected under various conditions. However, no single ‘best’ method seems to exist leading to the co‐occurrence of various approaches to study butterfly mobility, and therefore a high heterogeneity among data on dispersal across this group. Accordingly, we here reviewed the knowledge accumulated on dispersal and mobility in butterflies, to detect general patterns. This meta‐analysis specifically addressed two questions. Firstly, do the various methods provide a congruent picture of how dispersal ability is distributed across species? Secondly, is dispersal species‐specific? Five sources of data were analysed: multisite mark‐recapture experiments, genetic studies, experimental assessments, expert opinions, and transect surveys. We accounted for potential biases due to variation in genetic markers, sample sizes, spatial scales or the level of habitat fragmentation. We showed that the various dispersal estimates generally converged, and that the relative dispersal ability of species could reliably be predicted from their relative vagrancy (records of butterflies outside their normal habitat). Expert opinions gave much less reliable estimates of realized dispersal but instead reflected migration propensity of butterflies. Within‐species comparisons showed that genetic estimates were relatively invariable, while other dispersal estimates were highly variable. This latter point questions dispersal as a species‐specific, invariant trait.     

The Park Grass Experiment and next‐generation approaches: local adaptation of sweet vernal grass revisited

Long‐term ecological experiments provide unique opportunities to observe the effects of natural selection. The Park Grass Experiment at Rothamsted Experiment Station in Hertfordshire, UK, is the longest running ecological experiment that incorporates fertilization treatments and has been ongoing since 1856. In the 1970s, local adaptation was observed in the grass Anthoxanthum odoratum to the elevated soil aluminium levels of the fertilized plots. Gould et al. ( 2014 ) have utilized this system to reevaluate the extent of local adaptation, first documented nearly 45 years ago (Snaydon 1970 ), and to use emerging molecular approaches to identify candidate genes for the adaptation. From their work, they identify several plausible candidate loci for aluminium tolerance. This work shows the power of long‐term field‐based trials in a scientific age concentrated on rapidly emerging molecular techniques often utilized in short, narrowly focused laboratory or controlled environment experiments. The current study clearly illustrates the benefits gained by combining these molecular approaches within long‐term monitoring experiments that can be regularly revisited in a changing world and used to address questions on evolutionary scales.     

The genomic basis of adaptation to high‐altitude habitats in the eastern honey bee (Apis cerana)

The eastern honey bee (Apis cerana) is of central importance for agriculture in Asia. It has adapted to a wide variety of environmental conditions across its native range in southern and eastern Asia, which includes high‐altitude regions. eastern honey bees inhabiting mountains differ morphologically from neighbouring lowland populations and may also exhibit differences in physiology and behaviour. We compared the genomes of 60 eastern honey bees collected from high and low altitudes in Yunnan and Gansu provinces, China, to infer their evolutionary history and to identify candidate genes that may underlie adaptation to high altitude. Using a combination of F_ST‐based statistics, long‐range haplotype tests and population branch statistics, we identified several regions of the genome that appear to have been under positive selection. These candidate regions were strongly enriched for coding sequences and had high haplotype homozygosity and increased divergence specifically in highland bee populations, suggesting they have been subjected to recent selection in high‐altitude habitats. Candidate loci in these genomic regions included genes related to reproduction and feeding behaviour in honey bees. Functional investigation of these candidate loci is necessary to fully understand the mechanisms of adaptation to high‐altitude habitats in the eastern honey bee.     

Sex‐biased dispersal of human ancestors

Some anthropologists and primatologists have argued that, judging by extant chimpanzees and humans, which are female‐biased dispersers, the common ancestors of humans and chimpanzees were also female‐biased dispersers. It has been thought that sex‐biased dispersal patterns have been genetically transmitted for millions of years. However, this character has changed many times with changes in environment and life‐form during human evolution and historical times. I examined life‐form and social organization of nonhuman primates, among them gatherers (foragers), hunter‐gatherers, agriculturalists, industrialists, and modern and extant humans. I conclude that dispersal patterns changed in response to environmental conditions during primate and human evolution.     

The genetic basis of color‐related local adaptation in a ring‐like colonization around the Mediterranean

Uncovering the genetic basis of phenotypic variation and the population history under which it established is key to understand the trajectories along which local adaptation evolves. Here, we investigated the genetic basis and evolutionary history of a clinal plumage color polymorphism in European barn owls (Tyto alba). Our results suggest that barn owls colonized the Western Palearctic in a ring‐like manner around the Mediterranean and meet in secondary contact in Greece. Rufous coloration appears to be linked to a recently evolved nonsynonymous‐derived variant of the melanocortin 1 receptor (MC1R) gene, which according to quantitative genetic analyses evolved under local adaptation during or following the colonization of Central Europe. Admixture patterns and linkage disequilibrium between the neutral genetic background and color found exclusively within the secondary contact zone suggest limited introgression at secondary contact. These results from a system reminiscent of ring species provide a striking example of how local adaptation can evolve from derived genetic variation.     

Extent and scale of local adaptation in salmonid fishes: review and meta-analysis

What is the extent and scale of local adaptation (LA)? How quickly does LA arise? And what is its underlying molecular basis? Our review and meta-analysis on salmonid fishes estimates the frequency of LA to be ∼55–70%, with local populations having a 1.2 times average fitness advantage relative to foreign populations or to their performance in new environments. Salmonid LA is evident at a variety of spatial scales (for example, few km to>1000 km) and can manifest itself quickly (6–30 generations). As the geographic scale between populations increases, LA is generally more frequent and stronger. Yet the extent of LA in salmonids does not appear to differ from that in other assessed taxa. Moreover, the frequency with which foreign salmonid populations outperform local populations (∼23–35%) suggests that drift, gene flow and plasticity often limit or mediate LA. The relatively few studies based on candidate gene and genomewide analyses have identified footprints of selection at both small and large geographical scales, likely reflecting the specific functional properties of loci and the associated selection regimes (for example, local niche partitioning, pathogens, parasites, photoperiodicity and seasonal timing). The molecular basis of LA in salmonids is still largely unknown, but differential expression at the same few genes is implicated in the convergent evolution of certain phenotypes. Collectively, future research will benefit from an integration of classical and molecular approaches to understand: (i) species differences and how they originate, (ii) variation in adaptation across scales, life stages, population sizes and environmental gradients, and (iii) evolutionary responses to human activities.     

The effect of frequency‐dependent selection on resistance and tolerance to herbivory

Negative frequency‐dependent selection (FDS), where rare genotypes are favoured by selection, is commonly invoked as a mechanism explaining the maintenance of genetic variation in plant defences. However, empirical tests of FDS in plant–herbivore interactions are lacking. We evaluated whether the oviposition preference of the specialist herbivore Lema daturaphila is a mechanism through which this herbivore can exert FDS on its host plant Datura stramonium. The frequency of contrasting resistance–tolerance strategies was manipulated within experimental plots, and the plants were exposed to a similar initial density of their natural herbivore. Herbivore oviposition preference and final density, as well as plant damage and seed production, were estimated. Overall, we found that the high‐resistant–low‐tolerant genotypes produced four times more seeds when common than when rare, whereas the high‐tolerant–low‐resistant genotypes achieved twice its fitness when rare than when common. This pattern was the result of differential oviposition preferences. In addition, when the high‐resistant–low‐tolerant genotypes were common, there was a three‐fold decreased in herbivore final density which led to a decrease in damage level by 10%. Thus, in our experiment positive FDS seems to favour resistance over tolerance. We discuss how this result would change if the extent of herbivore local adaptation and damage modify the pattern of positive FDS acting on resistance and the optimal allocation to tolerance.     

Long‐distance dispersal maximizes evolutionary potential during rapid geographic range expansion

Conventional wisdom predicts that sequential founder events will cause genetic diversity to erode in species with expanding geographic ranges, limiting evolutionary potential at the range margin. Here, we show that invasive European starlings (Sturnus vulgaris) in South Africa preserve genetic diversity during range expansion, possibly as a result of frequent long‐distance dispersal events. We further show that unfavourable environmental conditions trigger enhanced dispersal, as indicated by signatures of selection detected across the expanding range. This brings genetic variation to the expansion front, counterbalancing the cumulative effects of sequential founding events and optimizing standing genetic diversity and thus evolutionary potential at range margins during spread. Therefore, dispersal strategies should be highlighted as key determinants of the ecological and evolutionary performances of species in novel environments and in response to global environmental change.     

The founding of Mauritian endemic coffee trees by a synchronous long‐distance dispersal event

The stochastic process of long‐distance dispersal is the exclusive means by which plants colonize oceanic islands. Baker's rule posits that self‐incompatible plant lineages are unlikely to successfully colonize oceanic islands because they must achieve a coordinated long‐distance dispersal of sufficiently numerous individuals to establish an outcrossing founder population. Here, we show for the first time that Mauritian Coffea species are self‐incompatible and thus represent an exception to Baker's rule. The genus Coffea (Rubiaceae) is composed of approximately 124 species with a paleotropical distribution. Phylogenetic evidence strongly supports a single colonization of the oceanic island of Mauritius from either Madagascar or Africa. We employ Bayesian divergence time analyses to show that the colonization of Mauritius was not a recent event. We genotype S‐RNase alleles from Mauritian endemic Coffea, and using S‐allele gene genealogies, we show that the Mauritian allelic diversity is confined to just seven deeply divergent Coffea S‐RNase allelic lineages. Based on these data, we developed an individual‐based model and performed a simulation study to estimate the most likely number of founding individuals involved in the colonization of Mauritius. Our simulations show that to explain the observed S‐RNase allelic diversity, the founding population was likely composed of fewer than 31 seeds that were likely synchronously dispersed from an ancestral mainland species.     

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.     

Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology

Gene flow among populations is typically thought to be antagonistic to population differentiation and local adaptation. However, this assumes that dispersing individuals disperse randomly with respect to their ability to use the environment. Yet dispersing individuals often sample and compare environments and settle in those environments that best match their phenotype, causing directed gene flow, which can in fact promote population differentiation and adaptation. We refer to this process as "matching habitat choice." Although this process has been acknowledged by several researchers, no synthesis or perspective on its potentially widespread importance exists. Here we synthesize empirical and theoretical studies, and offer a new perspective that matching habitat choice can have significant effects on important and controversial topics. We discuss the potential implications of matching habitat choice for the degree and rate of local adaptation, the evolution of niche width, adaptive peak shifts, speciation in the presence of gene flow, and on our view and interpretation of measures of natural selection. Because of its potential importance for such a wide range of topics, we call for heightened empirical and theoretical attention for this neglected dimension in evolutionary and ecological studies.     

The genetics of adaptation to discrete heterogeneous environments: frequent mutation or large‐effect alleles can allow range expansion

Range expansions are complex evolutionary and ecological processes. From an evolutionary standpoint, a populations' adaptive capacity can determine the success or failure of expansion. Using individual‐based simulations, we model range expansion over a two‐dimensional, approximately continuous landscape. We investigate the ability of populations to adapt across patchy environmental gradients and examine how the effect sizes of mutations influence the ability to adapt to novel environments during range expansion. We find that genetic architecture and landscape patchiness both have the ability to change the outcome of adaptation and expansion over the landscape. Adaptation to new environments succeeds via many mutations of small effect or few of large effect, but not via the intermediate between these cases. Higher genetic variance contributes to increased ability to adapt, but an alternative route of successful adaptation can proceed from low genetic variance scenarios with alleles of sufficiently large effect. Steeper environmental gradients can prevent adaptation and range expansion on both linear and patchy landscapes. When the landscape is partitioned into local patches with sharp changes in phenotypic optimum, the local magnitude of change between subsequent patches in the environment determines the success of adaptation to new patches during expansion.