The evolution of sexual imprinting through reinforcement*

Reinforcement is the process whereby assortative mating evolves due to selection against costly hybridization. Sexual imprinting could evolve as a mechanism of reinforcement, decreasing hybridization, or it could potentially increase hybridization in genetically purebred offspring of heterospecific social pairs. We use deterministic population genetic simulations to explore conditions under which sexual imprinting can evolve through reinforcement. We demonstrate that a sexual imprinting component of female preference can evolve as a one‐allele assortative mating mechanism by reducing the risk of hybridization, and is generally effective at causing trait divergence. However, imprinting often evolves to be a component rather than the sole determinant of female preference. The evolution of imprinting has the unexpected side effect of homogenizing existing innate preference, because the imprinted preference neutralizes any innate preference. We also find that the weight of the imprinting component may evolve to a lower value when migration and divergent selection are strong and the cost of hybridization is low; these conditions render hybridization adaptive for immigrant females because they can acquire locally adaptive genes by mating with local males. Together, these results suggest that sexual imprinting can itself evolve as part of the speciation process, and in doing so has the capacity to promote or retard divergence through complex interactions.     

Local adaptation in dispersal in multi‐resource landscapes

The distribution of resources in space has important consequences for the evolution of dispersal‐related traits. Dispersal moderates patterns of gene flow and, consequently, the potential for local adaptation to spatially differentiated resource types. We lack both models and experiments that evaluate how dispersal evolves in landscapes with multiple resources. Here, we investigate the evolution of dispersal in landscapes that contain two resource types that differ in their spatial autocorrelations. Individuals may possess ecological traits that give them a fitness advantage on one or the other resource. We find that resources differing in their spatial autocorrelation select for different optimal dispersal strategies and, further, that some multi‐resource landscapes can support the stable coexistence of distinct dispersal strategies. Whether divergence in dispersal strategies between resource specialists occurs depends on the underlying structure of the resources and the degree of linkage between dispersal strategies and ecological specialization. This work indicates that the spatial autocorrelation of resources is an important factor in determining when evolutionary branching is likely to occur, and sheds light on when secondary isolating mechanisms should arise between locally adapted specialists.     

HOW DOES POLLEN VERSUS SEED DISPERSAL AFFECT NICHE EVOLUTION?

In heterogeneous landscapes, the genetic and demographic consequences of dispersal influence the evolution of niche width. Unless pollen is limiting, pollen dispersal does not contribute directly to population growth. However, by disrupting local adaptation, it indirectly affects population dynamics. We compare the effect of pollen versus seed dispersal on the evolution of niche width in heterogeneous habitats, explicitly considering the feedback between maladaptation and demography. We consider two scenarios: the secondary contact of two subpopulations, in distinct, formerly isolated habitats, and the colonization of an empty habitat with dispersal between the new and ancestral habitat. With an analytical model, we identify critical levels of genetic variance leading to niche contraction (secondary contact scenario), or expansion (new habitat scenario). We confront these predictions with simulations where the genetic variance freely evolves. Niche contraction occurs when habitats are very different. It is faster as total gene flow increases or as pollen predominates in overall gene flow. Niche expansion occurs when habitat heterogeneity is not too high. Seed dispersal accelerates it, whereas pollen dispersal tends to retard it. In both scenarios very high seed dispersal leads to extinction. Overall, our results predict a wider niche for species dispersing seeds more than pollen.     

Mating timing,dispersal and local adaptation in patchy environments

Dispersal is a life‐history trait that can evolve under various known selective pressures as identified by a multitude of theoretical and empirical studies. Yet only few of them are considering the succession of mating and dispersal. The sequence of these events influences gene flow and consequently affects the dynamics and evolution of populations. We use individual‐based simulations to investigate the evolution of the timing of dispersal and mating, i.e. mating before or after dispersal. We assume a discrete insect metapopulation in a heterogeneous environment, where populations may adapt to local conditions and only females are allowed to disperse. We run the model assuming different levels of species habitat tolerance, carrying capacity, and temporal environmental variability. Our results show that in species with narrow habitat tolerance, low to moderate dispersal evolves in combination with mating after dispersal (post‐dispersal mating). With such a strategy dispersing females benefit from mating with a resident male, as their offspring will be better adapted to the local habitat conditions. On the contrary, in species with wide habitat tolerance higher dispersal rates in combination with pre‐dispersal mating evolves. In this case individuals are adapted to the ‘average’ habitat where pre‐dispersal mating conveys the benefit of carrying relatives’ genes into a new population. With high dispersal rates and large population size, local adaptation and kin structure both vanish and the temporal sequence of dispersal and mating may become a (nearly) neutral trait.     

PHENOTYPE-DEPENDENT NATIVE HABITAT PREFERENCE FACILITATES DIVERGENCE BETWEEN PARAPATRIC LAKE AND STREAM STICKLEBACK

Adaptive divergence between adjoining populations reflects a balance between the diversifying effect of divergent selection and the potentially homogenizing effect of gene flow. In most models of migration-selection balance, gene flow is assumed to reflect individuals' inherent capacity to disperse, without regard to the match between individuals' phenotypes and the available habitats. However, habitat preferences can reduce dispersal between contrasting habitats, thereby alleviating migration load and facilitating adaptive divergence. We tested whether habitat preferences contribute to adaptive divergence in a classic example of migration-selection balance: parapatric lake and stream populations of three-spine stickleback ( Gasterosteus aculeatus ). Using a mark-transplant-recapture experiment on morphologically divergent parapatric populations, we showed that 90% of lake and stream stickleback returned to their native habitat, reducing migration between habitats by 76%. Furthermore, we found that dispersal into a nonnative habitat was phenotype dependent. Stream fish moving into the lake were morphologically more lake-like than those returning to the stream (and the converse for lake fish entering the stream). The strong native habitat preference documented here increases the extent of adaptive divergence between populations two- to fivefold relative to expectations with random movement. These results illustrate the potential importance of adaptive habitat choice in driving parapatric divergence.     

The relative influence of natural selection and geography on gene flow in guppies

Two general processes may influence gene flow among populations. One involves divergent selection, wherein the maladaptation of immigrants and hybrids impedes gene flow between ecological environments (i.e. ecological speciation). The other involves geographic features that limit dispersal. We determined the relative influence of these two processes in natural populations of Trinidadian guppies (Poecilia reticulata). If selection is important, gene flow should be reduced between different selective environments. If geography is important, gene flow should be impeded by geographic distance and physical barriers. We examined how genetic divergence, long-term gene flow, and contemporary dispersal within a watershed were influenced by waterfalls, geographic distance, predation, and habitat features. We found that waterfalls and geographic distance increased genetic divergence and reduced dispersal and long-term gene flow. Differences in predation or habitat features did not influence genetic divergence or gene flow. In contrast, differences in predation did appear to reduce contemporary dispersal. We suggest that the standard predictions of ecological speciation may be heavily nuanced by the mating behaviour and life history strategies of guppies.     

Linking movement behaviour to dispersal and divergence in plethodontid salamanders

To better understand the evolutionary and ecological effects of dispersal, there is growing emphasis on the need to integrate direct data on movement behaviour into landscape-scale analyses. However, little is known about the general link between movement behaviour and large-scale patterns of dispersal and gene flow. Likewise, although recent studies suggest that nonrandom, directionally biased movement and dispersal can promote evolutionary divergence, the generality of this mechanism is unknown. We test the hypothesis that directionally biased movement and dispersal by plethodontid salamanders interact with the topography of headwater areas to affect genetic and phenotypic divergence. Movements by Gyrinophilus porphyriticus and Eurycea bislineata show contrasting directional biases: upstream bias in G. porphyriticus and downstream bias in E. bislineata. Consistent with predictions of how these biases interact with slope to affect dispersal and gene flow, genetic distance increased with slope in G. porphyriticus and decreased with slope in E. bislineata over a standardized distance of 1 km along six headwater streams. In both species, phenotypic divergence in relative trunk length was positively related to genetic divergence. These results indicate that landscape-scale patterns of dispersal and gene flow are closely related to movement behaviour in G. porphyriticus and E. bislineata, and underscore the value of information on movement behaviour for predicting and interpreting patterns of dispersal and gene flow in complex landscapes. This study also provides new evidence that directionally biased movement and dispersal can be important sources of intra- and interspecific variation in population divergence, and highlights the value of explicit, a priori predictions in landscape genetic studies.     

Contemporary ecotypic divergence during a recent range expansion was facilitated by adaptive introgression

Although rapid phenotypic evolution during range expansion associated with colonization of contrasting habitats has been documented in several taxa, the evolutionary mechanisms that underlie such phenotypic divergence have less often been investigated. A strong candidate for rapid ecotype formation within an invaded range is the three‐spine stickleback in the Lake Geneva region of central Europe. Since its introduction only about 140 years ago, it has undergone a significant expansion of its range and its niche, now forming phenotypically differentiated parapatric ecotypes that occupy either the pelagic zone of the large lake or small inlet streams, respectively. By comparing museum collections from different times with contemporary population samples, we here reconstruct the evolution of parapatric phenotypic divergence through time. Using genetic data from modern samples, we infer the underlying invasion history. We find that parapatric habitat‐dependent phenotypic divergence between the lake and stream was already present in the first half of the twentieth century, but the magnitude of differentiation increased through time, particularly in antipredator defence traits. This suggests that divergent selection between the habitats occurred and was stable through much of the time since colonization. Recently, increased phenotypic differentiation in antipredator defence traits likely results from habitat‐dependent selection on alleles that arrived through introgression from a distantly related lineage from outside the Lake Geneva region. This illustrates how hybridization can quickly promote phenotypic divergence in a system where adaptation from standing genetic variation was constrained.     

Matching habitat choice promotes species persistence under climate change

Species may survive under contemporary climate change by either shifting their range or adapting locally to the warmer conditions. Theoretical and empirical studies recently underlined that dispersal, the central mechanism behind these responses, may depend on the match between an individuals’ phenotype and local environment. Such matching habitat choice is expected to induce an adaptive gene flow, but it now remains to be studied whether this local process could promote species’ responses to climate change. Here, we investigate this by developing an individual‐based model including either random dispersal or temperature‐dependent matching habitat choice. We monitored population composition and distribution through space and time under climate change. Relative to random dispersal, matching habitat choice induced an adaptive gene flow that lessened spatial range loss during climate warming by improving populations’ viability within the range (i.e. limiting range fragmentation) and by facilitating colonization of new habitats at the cold margin. The model even predicted range contraction under random dispersal but range expansion under optimal matching habitat choice. These benefits of matching habitat choice for population persistence mostly resulted from adaptive immigration decision and were greater for populations with larger dispersal distance and higher emigration probability. We also found that environmental stochasticity resulted in suboptimal matching habitat choice, decreasing the benefits of this dispersal mode under climate change. However population persistence was still better under suboptimal matching habitat choice than under random dispersal. Our results highlight the urgent need to implement more realistic mechanisms of dispersal such as matching habitat choice into models predicting the impacts of ongoing climate change on biodiversity.     

Urbanisation versus agriculture: a comparison of local genetic diversity and gene flow between wood mouse Apodemus sylvaticus populations in human‐modified landscapes

Urbanisation and agriculture dramatically modify the landscapes available for use by wildlife, affecting key aspects of their ecology such as survival, foraging, predation, competition and reproductive success. Relatively little is known about the effects of urbanisation and agriculture on the genetic structure, gene flow and genetic diversity of wild species. Here, landscape genetic techniques were applied to compare local genetic diversity and gene flow between wood mouse populations in urban and arable landscapes. Using nine microsatellite markers, individuals were genotyped from six arable and seven urban sample sites. Inter‐population genetic differentiation was significantly greater in urban than arable habitat, while allele richness, private allele richness and heterozygosity were higher for arable sample sites, with varying degrees of significance. These suggest that urban habitat was sufficiently fragmented to limit gene flow. To test the effect of landscape features on gene flow, several cost‐distance measures were generated. Overland distance and Euclidean distance correlated best with inter‐population genetic differentiation in arable habitat, whereas distances that accommodated differences in habitat quality better explained differentiation in urban habitat. There was no evidence that margins adjacent to roads, rivers or railways facilitated gene flow. Together, the results indicate that urban landscapes expose wood mice to greater fragmentation in habitat quality than arable areas, leading to greater population isolation that is not mitigated by the presence of dispersal corridors.     

Dispersal ability and habitat requirements determine landscape‐level genetic patterns in desert aquatic insects

Species occupying the same geographic range can exhibit remarkably different population structures across the landscape, ranging from highly diversified to panmictic. Given limitations on collecting population‐level data for large numbers of species, ecologists seek to identify proximate organismal traits—such as dispersal ability, habitat preference and life history—that are strong predictors of realized population structure. We examined how dispersal ability and habitat structure affect the regional balance of gene flow and genetic drift within three aquatic insects that represent the range of dispersal abilities and habitat requirements observed in desert stream insect communities. For each species, we tested for linear relationships between genetic distances and geographic distances using Euclidean and landscape‐based metrics of resistance. We found that the moderate‐disperser Mesocapnia arizonensis (Plecoptera: Capniidae) has a strong isolation‐by‐distance pattern, suggesting migration–drift equilibrium. By contrast, population structure in the flightless Abedus herberti (Hemiptera: Belostomatidae) is influenced by genetic drift, while gene flow is the dominant force in the strong‐flying Boreonectes aequinoctialis (Coleoptera: Dytiscidae). The best‐fitting landscape model for M. arizonensis was based on Euclidean distance. Analyses also identified a strong spatial scale‐dependence, where landscape genetic methods only performed well for species that were intermediate in dispersal ability. Our results highlight the fact that when either gene flow or genetic drift dominates in shaping population structure, no detectable relationship between genetic and geographic distances is expected at certain spatial scales. This study provides insight into how gene flow and drift interact at the regional scale for these insects as well as the organisms that share similar habitats and dispersal abilities.     

Song divergence and male dispersal among bird populations: a spatially explicit model testing the role of vocal learning

The importance of bird song in sexual selection and the widespread existence of geographical variation in song has raised the question of whether dialects can promote the evolution of new, reproductively isolated, subgroups. However, the effect of song learning on the relation between song divergence and gene flow is still poorly understood. We explored the origin and maintenance of song divergence and its consequences for male dispersal between populations. To do this, we used a spatially explicit model to study the effect of vocal learning mode (predispersal and postdispersal) and the role of intrasexual selection among males. The majority of scenarios simulated in the model led to significant genetic and phenotypic song divergence, consistent with the widespread occurrence of dialects in natural populations. Intrasexual selection in the form of male exclusion, dependent on song matching between neighbours, was an efficient mechanism driving song divergence. Most importantly, song learning was decisive in causing an incongruence of genetic divergence and song divergence between populations. As a consequence, song learning often prevented the expected negative relation between the degree of song divergence and dispersal. These findings may help to interpret empirical data on song divergence and gene flow and provide qualitative and testable predictions for conditions under which intraspecific song variation may promote reproductive divergence and speciation. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Habitat connectivity is determined by the scale of habitat loss and dispersal strategy

Understanding factors that ameliorate the impact of habitat loss is a major focus of conservation research. One key factor influencing species persistence and evolution is the ability to disperse across increasingly patchy landscapes. Here we ask whether interpatch distance (a proxy for habitat loss) and dispersal strategy can interact to form thresholds where connectivity breaks down. We assayed dispersal across a range of interpatch distances in fruit flies carrying allelic variants of a gene known to underlie differences in dispersal strategy. Dispersal‐limited flies experienced a distinct negative threshold in connectivity at greater interpatch distances, and this was not observed in more dispersive flies. Consequently, this differential response of dispersal‐limited and more dispersive flies to decreasing connectivity suggests that habitat loss could have important implications on the evolution and maintenance of genetic variation underlying dispersal strategy.     

Evolutionary divergence in freshwater insects with contrasting dispersal capacity across a sea of desert

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Comparing the consequences of natural selection,adaptive phenotypic plasticity,and matching habitat choice for phenotype–environment matching,population genetic structure,and reproductive isolation in meta‐populations

Organisms commonly experience significant spatiotemporal variation in their environments. In response to such heterogeneity, different mechanisms may act that enhance ecological performance locally. However, depending on the nature of the mechanism involved, the consequences for populations may differ greatly. Building on a previous model that investigated the conditions under which different adaptive mechanisms (co)evolve, this study compares the ecological and evolutionary population consequences of three very different responses to environmental heterogeneity: matching habitat choice (directed gene flow), adaptive plasticity (associated with random gene flow), and divergent natural selection. Using individual‐based simulations, we show that matching habitat choice can have a greater adaptive potential than plasticity or natural selection: it allows for local adaptation while protecting genetic polymorphism despite global mating or strong environmental changes. Our simulations further reveal that increasing environmental fluctuations and unpredictability generally favor the emergence of specialist genotypes but that matching habitat choice is better at preventing local maladaptation by individuals. This confirms that matching habitat choice can speed up the genetic divergence among populations, cause indirect assortative mating via spatial clustering, and hence even facilitate sympatric speciation. This study highlights the potential importance of directed dispersal in local adaptation and speciation, stresses the difficulty of deriving its operation from nonexperimental observational data alone, and helps define a set of ecological conditions which should favor its emergence and subsequent detection in nature.     

Extreme genetic structure in a social bird species despite high dispersal capacity

Social barriers have been shown to reduce gene flow and contribute to genetic structure among populations in species with high cognitive capacity and complex societies, such as cetaceans, apes and humans. In birds, high dispersal capacity is thought to prevent population divergence unless major geographical or habitat barriers induce isolation patterns by dispersal, colonization or adaptation limitation. We report that Iberian populations of the red‐billed chough, a social, gregarious corvid with high dispersal capacity, show a striking degree of genetic structure composed of at least 15 distinct genetic units. Monitoring of marked individuals over 30 years revealed that long‐distance movements over hundreds of kilometres are common, yet recruitment into breeding populations is infrequent and highly philopatric. Genetic differentiation is weakly related to geographical distance, and habitat types used are overall qualitatively similar among regions and regularly shared by individuals of different populations, so that genetic structure is unlikely to be due solely to isolation by distance or isolation by adaptation. Moreover, most population nuclei showed relatively high levels of genetic diversity, suggesting a limited role for genetic drift in significantly differentiating populations. We propose that social mechanisms may underlie this unprecedented level of genetic structure in birds through a pattern of isolation by social barriers not yet described, which may have driven this remarkable population divergence in the absence of geographical and environmental barriers.     

Do different rates of gene flow underlie variation in phenotypic and phenological clines in a montane grasshopper community?

Species responses to environmental change are likely to depend on existing genetic and phenotypic variation, as well as evolutionary potential. A key challenge is to determine whether gene flow might facilitate or impede genomic divergence among populations responding to environmental change, and if emergent phenotypic variation is dependent on gene flow rates. A general expectation is that patterns of genetic differentiation in a set of codistributed species reflect differences in dispersal ability. In less dispersive species, we predict greater genetic divergence and reduced gene flow. This could lead to covariation in life‐history traits due to local adaptation, although plasticity or drift could mirror these patterns. We compare genome‐wide patterns of genetic structure in four phenotypically variable grasshopper species along a steep elevation gradient near Boulder, Colorado, and test the hypothesis that genomic differentiation is greater in short‐winged grasshopper species, and statistically associated with variation in growth, reproductive, and physiological traits along this gradient. In addition, we estimate rates of gene flow under competing demographic models, as well as potential gene flow through surveys of phenological overlap among populations within a species. All species exhibit genetic structure along the elevation gradient and limited gene flow. The most pronounced genetic divergence appears in short‐winged (less dispersive) species, which also exhibit less phenological overlap among populations. A high‐elevation population of the most widespread species, Melanoplus sanguinipes, appears to be a sink population derived from low elevation populations. While dispersal ability has a clear connection to the genetic structure in different species, genetic distance does not predict growth, reproductive, or physiological trait variation in any species, requiring further investigation to clearly link phenotypic divergence to local adaptation.     

Differences in rheotactic responses contribute to divergent habitat use between parapatric lake and stream threespine stickleback

Migration among populations is widely thought to undermine adaptive divergence, assuming gene flow arises from random movement of individuals. If individuals instead differ in dispersal behavior, phenotype‐dependent dispersal can reduce the effective rate of gene flow or even facilitate divergence. For example, parapatric populations of lake and stream stickleback tend to actively avoid dispersing into the adjoining habitat. However, the behavioral basis of this nonrandom dispersal was previously unknown. Here, we show that lake and stream stickleback exhibit divergent rheotactic responses (behavioral response to currents). During the breeding season, wild‐caught inlet stream stickleback were better than lake fish at maintaining position in currents, faced upstream more, and spent more time in low‐current areas. As a result, stream fish expended significantly less energy in currents than did lake fish. These divergent rheotactic responses likely contribute to divergent habitat use by lake and stream stickleback. Although rheotactic differences were absent in nonbreeding fish, divergent behavior of breeding‐season fish may suffice for assortative mating by breeding location. The resulting reproductive isolation between lake and stream fish may explain the fine‐scale evolutionary differentiation in parapatric stickleback populations.     

Food choice behaviour may promote habitat specificity in mixed populations of clonal and sexual Potamopyrgus antipodarum

Genetic polymorphism along an environmental gradient may be maintained if disruptive selection on habitat-specific traits leads to a correlated response in traits that reduce gene flow between habitats. We studied a short-distance cline in a population of freshwater snails Potamopyrgus antipodarum in which sexual and clonal snails coexist. Sexuals and clones show a life history cline by depth: snails reproduce at a smaller size in shallower habitats. Clones are also structured genetically across habitats and seem not to mix, even though habitats are within the dispersal distance of the snails and the opportunity for gene flow via migration must be considerable. Because habitat preference may promote divergence in both clones and sexuals along the depth gradient, we investigated whether snails show habitat-specific food choice behaviour that could reduce migration. We tested the food choice behaviour of the snails by exposing them simultaneously to food from their home and adjacent habitats. Both juvenile and adult snails from the shallow shore bank and a mid-water macrophyte habitat preferentially grazed on the vegetation of their original habitats. We suggest that the observed genetic and life history cline may be maintained by food choice behaviour that may promote a partial barrier to gene flow between the habitats. Copyright 2000 The Association for the Study of Animal Behaviour.     

The role of recombination,niche‐specific gene pools and flexible genomes in the ecological speciation of bacteria

Bacteria diversify into genetic clusters analogous to those observed in sexual eukaryotes, but the definition of bacterial species is an ongoing problem. Recent work has focused on adaptation to distinct ecological niches as the main driver of clustering, but there remains debate about the role of recombination in that process. One view is that homologous recombination occurs too rarely for gene flow to constrain divergent selection. Another view is that homologous recombination is frequent enough in many bacterial populations that barriers to gene flow are needed to permit divergence. Niche‐specific gene pools have been proposed as a general mechanism to limit gene flow. We use theoretical models to evaluate additional hypotheses that evolving genetic architecture, specifically the effect sizes of genes and gene gain and loss, can limit gene flow between diverging populations. Our model predicts that (a) in the presence of gene flow and recombination, ecological divergence is concentrated in few loci of large effect and (b) high rates of gene flow plus recombination promote gene loss and favor the evolution of niche‐specific genes. The results show that changing genetic architecture and gene loss can facilitate ecological divergence, even without niche‐specific gene pools. We discuss these results in the context of recent studies of sympatric divergence in microbes.