Mutation surfing and the evolution of dispersal during range expansions

A growing body of empirical evidence demonstrates that at an expanding front, there can be strong selection for greater dispersal propensity, whereas recent theory indicates that mutations occurring towards the front of a spatially expanding population can sometimes ‘surf’ to high frequency and spatial extent. Here, we consider the potential interplay between these two processes: what role may mutation surfing play in determining the course of dispersal evolution and how might dispersal evolution itself influence mutation surfing? Using an individual‐based coupled‐map lattice model, we first run simulations to determine the fate of dispersal mutants that occur at an expanding front. Our results highlight that mutants that have a slightly higher dispersal propensity than the wild type always have a higher survival probability than those mutants with a dispersal propensity lower than, or very similar to, the wild type. However, it is not always the case that mutants with very high dispersal propensity have the greatest survival probability. When dispersal mortality is high, mutants of intermediate dispersal survive most often. Interestingly, the rate of dispersal that ultimately evolves at an expanding front is often substantially higher than that which confers a novel mutant with the greatest probability of survival. Second, we run a model in which we allow dispersal to evolve over the course of a range expansion and ask how the fate of a neutral or nonneutral mutant depends upon when and where during the expansion it arises. These simulations highlight that the success of a neutral mutant depends upon the dispersal genotypes that it is associated with. An important consequence of this is that novel mutants that arise at the front of an expansion, and survive, typically end up being associated with more dispersive genotypes than the wild type. These results offer some new insights into causes and the consequences of dispersal evolution during range expansions, and the methodology we have employed can be readily extended to explore the evolutionary dynamics of other life history characteristics.     

Spatially explicit models of divergence and genome hitchhiking

Strong barriers to genetic exchange can exist at divergently selected loci, whereas alleles at neutral loci flow more readily between populations, thus impeding divergence and speciation in the face of gene flow. However, ‘divergence hitchhiking’ theory posits that divergent selection can generate large regions of differentiation around selected loci. ‘Genome hitchhiking’ theory suggests that selection can also cause reductions in average genome‐wide rates of gene flow, resulting in widespread genomic divergence (rather than divergence only around specific selected loci). Spatial heterogeneity is ubiquitous in nature, yet previous models of genetic barriers to gene flow have explored limited combinations of spatial and selective scenarios. Using simulations of secondary contact of populations, we explore barriers to gene flow in various selective and spatial contexts in continuous, two‐dimensional, spatially explicit environments. In general, the effects of hitchhiking are strongest in environments with regular spatial patterning of starkly divergent habitat types. When divergent selection is very strong, the absence of intermediate habitat types increases the effects of hitchhiking. However, when selection is moderate or weak, regular (vs. random) spatial arrangement of habitat types becomes more important than the presence of intermediate habitats per se. We also document counterintuitive processes arising from the stochastic interplay between selection, gene flow and drift. Our results indicate that generalization of results from two‐deme models requires caution and increase understanding of the genomic and geographic basis of population divergence.     

Genetic variance for behavioural ‘predictability’ of stress response

Genetic factors underpinning phenotypic variation are required if natural selection is to result in adaptive evolution. However, evolutionary and behavioural ecologists typically focus on variation among individuals in their average trait values and seek to characterize genetic contributions to this. As a result, less attention has been paid to if and how genes could contribute towards within‐individual variance or trait ‘predictability’. In fact, phenotypic ‘predictability’ can vary among individuals, and emerging evidence from livestock genetics suggests this can be due to genetic factors. Here, we test this empirically using repeated measures of a behavioural stress response trait in a pedigreed population of wild‐type guppies. We ask (a) whether individuals differ in behavioural predictability and (b) whether this variation is heritable and so evolvable under selection. Using statistical methodology from the field of quantitative genetics, we find support for both hypotheses and also show evidence of a genetic correlation structure between the behavioural trait mean and individual predictability. We show that investigating sources of variability in trait predictability is statistically tractable and can yield useful biological interpretation. We conclude that, if widespread, genetic variance for ‘predictability’ will have major implications for the evolutionary causes and consequences of phenotypic variation.     

When can ecological speciation be detected with neutral loci?

It is not yet clear under what conditions empirical studies can reliably detect progress toward ecological speciation through the analysis of allelic variation at neutral loci. We use a simulation approach to investigate the range of parameter space under which such detection is, and is not, likely. We specifically test for the conditions under which divergent natural selection can cause a ‘generalized barrier to gene flow’ that is present across the genome. Our individual‐based numerical simulations focus on how population divergence at neutral loci varies in relation to recombination rate with a selected locus, divergent selection on that locus, migration rate and population size. We specifically test whether genetic differences at neutral markers are greater between populations in different environments than between populations in similar environments. We find that this expected signature of ecological speciation can be detected under part of the parameter space, most consistently when divergent selection is strong and migration is intermediate. By contrast, the expected signature of ecological speciation is not reliably detected when divergent selection is weak or migration is low or high. These findings provide insights into the strengths and weaknesses of using neutral markers to infer ecological speciation in natural systems.     

Characterising extinction debt following habitat fragmentation using neutral theory

Habitat loss leads to species extinctions, both immediately and over the long term as ‘extinction debt’ is repaid. The same quantity of habitat can be lost in different spatial patterns with varying habitat fragmentation. How this translates to species loss remains an open problem requiring an understanding of the interplay between community dynamics and habitat structure across temporal and spatial scales. Here we develop formulas that characterise extinction debt in a spatial neutral model after habitat loss and fragmentation. Central to our formulas are two new metrics, which depend on properties of the taxa and landscape: ‘effective area’, measuring the remaining number of individuals and ‘effective connectivity’, measuring individuals’ ability to disperse through fragmented habitat. This formalises the conventional wisdom that habitat area and habitat connectivity are the two critical requirements for long‐term preservation of biodiversity. Our approach suggests that mechanistic fragmentation metrics help resolve debates about fragmentation and species loss.     

The logic of asymmetric contests

A theoretical analysis is made of the evolution of behavioural strategies in contest situations. It is assumed that behaviour will evolve so as to maximize individual fitness. If so, a population will evolve an ‘evolutionarily stable strategy’, or ESS, which can be defined as a strategy such that, if all members of a population adopt it, no ‘mutant’ strategy can do better. A number of simple models of contest situations are analysed from this point of view. It is concluded that in ‘symmetric’ contests the ESS is likely to be a ‘mixed’ strategy; that is, either the population will be genetically polymorphic or individuals will be behaviourally variable. Most real contests are probably asymmetric, either in pay-off to the contestants, or in size or weapons, or in some ‘uncorrelated’ fashion; i.e. in a fashion which does not substantially bias either the pay-offs or the likely outcome of an escalated contest. An example of an uncorrelated asymmetry is that between the ‘discoverer’ of a resource and a ‘late-comer’. It is shown that the ESS in asymmetric contests will usually be to permit the asymmetric cue to settle the contest without escalation. Escalated contests will, however, occur if information to the contestants about the asymmetry is imperfect.     

Use of restriction fragment length polymorphisms for genetic counseling: Population genetic considerations

Two-locus population genetic models are analyzed to evaluate the utility of restriction fragment length polymorphisms for purposes of genetic counseling. It is shown that the linkage disequilibrium between a neutral marker and a tightly linked overdominant mutant will increase rapidly as the mutant moves to its polymorphic equilibrium. The linkage disequilibrium decays for deleterious recessive mutants. Two measures involving the linkage disequilibrium are investigated to determine how much information the transmission of the neutral marker provides about the transmission of the selected gene. In certain kinds of matings, where the parental two-locus genotypes and linkage phases are known, it is possible to determine whether or not a progeny is homozygous for the selected gene on the basis of the fetal genotype at the marker locus. A quantity of primary interest is the fraction of matings between individuals heterozygous for the selected gene in which exact diagnosis can be made in this way. The expected proportion of such matings, taken over all two-locus matings involving heterozygotes at the selected locus, is calculated as a function of the gene frequencies at the two loci and the linkage disequilibrium between them. This expected value is maximized when the linkage disequilibrium is at its maximum in absolute value. Fewer than half of all matings are informative if the linkage disequilibrium is small in magnitude or if the gene frequencies at the two loci are quite different. Consideration is also given to various conditional measures of association that may be useful when the parental two-locus genotypes are unknown. The results suggest that the utility of tightly linked neutral marker genes in predicting the transmission of a selected gene is generally less when selection acts against a recessive gene than for overdominant selection.     

Inertia: the discrepancy between individual and common good in dispersal and prospecting behaviour

The group selection debate of the 1960s made it clear that evolution does not necessarily increase population performance. Individuals can be selected to have traits that diminish a common good and make population persistence difficult. At the extreme, the discrepancy between levels of selection is predicted to make traits evolve towards values at which a population can no longer persist (evolutionary suicide). Dispersal and prospecting are prime examples of traits that have a strong influence on population persistence under environmental and demographic stochasticity. Theory predicts that an ‘optimal’ dispersal strategy from a population point of view can differ considerably from that produced by individual‐level selection. Because dispersal is frequently risky or otherwise costly, individuals are often predicted to disperse less than would be ideal for population performance (persistence or size). We define this discrepancy as ‘inertia’ and examine current knowledge of its occurrence and effects on population dynamics in nature. We argue that inertia is potentially widespread but that a framework is currently lacking for predicting precisely the extent to which it has a real influence on population persistence. The opposite of inertia, ‘hypermobility’ (more dispersal by individuals than would maximize population performance) remains a possibility: it is known that highest dispersal rates do not lead to best expected population performance, and examples of such high dispersal evolving exist at least in the theoretical literature. We also show, by considering prospecting behaviour, that similar issues arise in species with advanced cognitive and learning abilities. Individual prospecting strategies and the information acquired during dispersal are known to influence the decisions and therefore the fate of individuals and, as a corollary, populations. Again, the willingness of individuals to sample environments might evolve to levels that are not optimal for populations. This conflict can take intriguing forms. For example, better cognitive abilities of individuals may not always lead to better population‐level performance. Simulation studies have found that ‘blind’ dispersal can lead to better connected metapopulations than cognitively more advanced habitat choice rules: the latter can lead to too many individuals sticking to nearby safe habitat. The study of the mismatch between individual and population fitness should not be a mere intellectual exercise. Population managers typically need to take a population‐level view of performance, which may necessitate human intervention if it differs from what is selected for. We conclude that our knowledge of inertia and hypermobility would advance faster if theoretical studies—without much additional effort—quantified the population consequences of the evolving traits and compared this with hypothetical (not selectively favoured) dispersal rules, and if empirical studies were similarly conducted with the differing levels of selection in mind.     

Survival rates of mutant genes under artificial selection using individual and family information

We have used diffusion and branching process methods to investigate fixation rates, probabilities of survival per generation, and times to fixation of mutant genes under different selection methods incorporating individual and family information. Diffusion approximations fit well to simulated results even for large selection coefficients. Methods that give much weight to family information, such as BLUP evaluation which is widely used in animal breeding, reduce fixation rates of mutant genes because of the reduced effective population sizes. In general, it is observed that even mutants with relatively small heterozygous effects (say 0.1 phenotypic standard deviation) are practically ‘safe’ (i.e. their probability of loss from one generation to the next is smaller than, say, 10%) after just a few generations, typically less than 10. For methods of selection with larger effective size, such as within-family selection, the mutant is ‘safe’ in the population somewhat earlier but eventual fixation takes a longer time. Finally we evaluate the amount by which the use of marker assisted selection reduces the fixation probability of newly arisen mutants.     

Directionality of contact networks suppresses selection pressure in evolutionary dynamics

Individuals of different types, may it be genetic, cultural, or else, with different levels of fitness often compete for reproduction and survival. A fitter type generally has higher chances of disseminating their copies to other individuals. The fixation probability of a single mutant type introduced in a population of wild-type individuals quantifies how likely the mutant type spreads. How much the excess fitness of the mutant type increases its fixation probability, namely, the selection pressure, is important in assessing the impact of the introduced mutant. Previous studies mostly based on undirected and unweighted contact networks of individuals showed that the selection pressure depends on the structure of networks and the rule of reproduction. Real networks underlying ecological and social interactions are usually directed or weighted. Here we examine how the selection pressure is modulated by directionality of interactions under several update rules. Our conclusions are twofold. First, directionality discounts the selection pressure for different networks and update rules. Second, given a network, the update rules in which death events precede reproduction events significantly decrease the selection pressure than the other rules.     

Sensory trait variation contributes to biased dispersal of threespine stickleback in flowing water

Gene flow is widely thought to homogenize spatially separate populations, eroding effects of divergent selection. The resulting theory of ‘migration–selection balance’ is predicated on a common assumption that all genotypes are equally prone to dispersal. If instead certain genotypes are disproportionately likely to disperse, then migration can actually promote population divergence. For example, previous work has shown that threespine stickleback (Gasterosteus aculeatus) differ in their propensity to move up‐ or downstream (‘rheotactic response’), which may facilitate genetic divergence between adjoining lake and stream populations of stickleback. Here, we demonstrate that intraspecific variation in a sensory system (superficial neuromast lines) contributes to this variation in swimming behaviour in stickleback. First, we show that intact neuromasts are necessary for a typical rheotactic response. Next, we showed that there is heritable variation in the number of neuromasts and that stickleback with more neuromasts are more likely to move downstream. Variation in pectoral fin shape contributes to additional variation in rheotactic response. These results illustrate how within‐population quantitative variation in sensory and locomotor traits can influence dispersal behaviour, thereby biasing dispersal between habitats and favouring population divergence.     

Inheritance of vector competence by the thrips Ceratothripoides claratris (Shumsher) (Thysanoptera: Thripidae)

The thrips Ceratothripoides claratris is an efficient vector of the Capsicum chlorosis virus (CaCV). Transmission studies with a natural population of C. claratris found in a greenhouse ‘GH’ and a ‘colony’ derived from this ‘GH’ population by selection and inbreeding resulted in lowering the percentage of viruliferous individuals within the ‘colony’. After passing through approximately 20 generations, the ‘colony’ lost the ability to transmit the CaCV. When either viruliferous or non‐viruliferous virgin females reproduced parthenogenetically, 81% of F1 arrhenotokous males inherited their viruliferous status from their mothers, whilst, no viruliferous offspring arose from non‐viruliferous virgin mothers. Crosses between viruliferous and non‐viruliferous individuals suggest that the competence of the thrips C. claratris as a vector for this virus is probably a heritable trait controlled by a recessive allele.     

The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication

Wild and cultivated plants represent very different habitats for pathogens, especially when cultivated plants bear qualitative resistance genes. Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deployment of resistant cultivars. We studied one of the main poplar diseases, poplar rust, caused by the fungus Melampsora larici‐populina. A thousand and fifty individuals sampled from several locations in France were phenotyped for their virulence profile (ability to infect or not the most deployed resistant cultivar ‘Beaupré’), and a subset of these was genotyped using 25 microsatellite markers. Bayesian assignment tests on genetic data clustered the 476 genotyped individuals into three genetic groups. Group 1 gathered most virulent individuals and displayed evidence for selection and drastic demographic changes resulting from breakdown of the poplar cultivar ‘Beaupré’. Group 2 comprised individuals corresponding to ancestral populations of M. larici‐populina naturally occurring in the native range. Group 3 displayed the hallmarks of strict asexual reproduction, which has never previously been demonstrated in this species. We discuss how poplar cultivation has influenced the spatial and genetic structure of this plant pathogenic fungus, and has led to the spread of virulence alleles (gene swamping) in M. larici‐populina populations evolving on the wild host.     

Landscape‐scale variation in an anthropogenic factor shapes immune gene variation within a wild population

Understanding the spatial scale at which selection acts upon adaptive genetic variation in natural populations is fundamental to our understanding of evolutionary ecology, and has important ramifications for conservation. The environmental factors to which individuals of a population are exposed can vary at fine spatial scales, potentially generating localized patterns of adaptation. Here, we compared patterns of neutral and major histocompatibility complex (MHC) variation within an island population of Berthelot's pipit (Anthus berthelotii) to assess whether landscape‐level differences in pathogen‐mediated selection generate fine‐scale spatial structuring in these immune genes. Specifically, we tested for spatial associations between the distribution of avian malaria, and the factors previously shown to influence that distribution, and MHC variation within resident individuals. Although we found no overall genetic structure across the population for either neutral or MHC loci, we did find localized associations between environmental factors and MHC variation. One MHC class I allele (ANBE48) was directly associated with malaria infection risk, while the presence of the ANBE48 and ANBE38 alleles within individuals correlated (positively and negatively, respectively) with distance to the nearest poultry farm, an anthropogenic factor previously shown to be an important determinant of disease distribution in the study population. Our findings highlight the importance of considering small spatial scales when studying the patterns and processes involved in evolution at adaptive loci.     

Neoproterozoic 'snowball Earth' glaciations and the evolution of altruism

We hypothesize that a demographic and ecological effect of Neoproterozoic ‘snowball Earth’ glaciations was to increase the fitness of group‐level traits and consequently the likelihood of the evolution of macroscopic form. Extreme and repeated founder effects raised genetic relatedness – and therefore the influence of kin selection on the individuals within a group. This was permissive for the evolution of some highly costly altruistic traits, including those for macroscopic differentiation. In some eukaryotic species, the harsh and fluctuating abiotic conditions made a macroscopic physiology advantageous, perhaps necessary, for collective survival. This caused population‐wide group viability selection, whereby non‐altruist ‘cheat’ genotypes killed the groups they were in, and therefore themselves, by reaching fixation. Furthermore, dispersal between refugia would reach zero under anything near a ‘hard snowball’, which would protect altruists at high local frequency from the influx of cheats from neighbouring groups. We illustrate our hypothesis analytically and with a simple spatial model. We show how removal of between‐group dispersal, in a population with initial between‐group variation in cheat frequency, causes the relative frequency of altruists to increase while the population as a whole decreases in size, as a result of group death caused by cheat invasion. This may be of particular relevance to animal multicellularity because irreversible differentiation (highly altruistic in that it imposes a high fitness cost on the individual cell) is more prevalent than in other multicellular eukaryotes. The relevance of our hypothesis should be scaled by any future consensus on the severity of snowball Earth, but it is theoretically plausible that global‐scale glaciations had a systematic influence on the level of selection during Earth history.     

The effects of competition on the strength and softness of selection

Deleterious alleles are constantly introduced into populations due to mutation. In subdivided populations, the impact of these mutations depends on the strength of selection as well as the softness of selection, that is, the extent to which fitness is governed by local rather than global competition. It is widely appreciated that the intensity and type of competition will affect selection on deleterious mutations but most empirical work has focused solely on the effects of competition on selection strength. However, competition has rarely been studied in the context of selection ‘softness’ even though competition is at the conceptual root of soft selection. All other things being equal, theory predicts that inter‐ and intraspecific competitions have opposing effects on the softness of selection. Using Drosophila melanogaster, we estimated the strength and softness of selection in a ‘baseline’ competitive environment as well as two additional competitive environments characterized by either additional intra‐ or interspecific competitors. We found that competitive environment had little effect on the average strength of selection. While the softness of selection was affected by the type of competition, the direction of change varied across tests of different genes, contrary to expectation. Although the ‘hard/soft’ selection paradigm implicitly assumes that all individuals are equally sensitive to the local competitive environment, we found this not to be the case. Wild‐type individuals were more sensitive to changes in the genetic quality of their local competitors than mutant individuals.     

Spatial scaling of population synchrony in marine fish depends on their life history

The synchrony of population dynamics in space has important implications for ecological processes, for example affecting the spread of diseases, spatial distributions and risk of extinction. Here, we studied the relationship between spatial scaling in population dynamics and species position along the slow‐fast continuum of life history variation. Specifically, we explored how generation time, growth rate and mortality rate predicted the spatial scaling of abundance and yearly changes in abundance of eight marine fish species. Our results show that population dynamics of species' with ‘slow’ life histories are synchronised over greater distances than those of species with ‘fast’ life histories. These findings provide evidence for a relationship between the position of the species along the life history continuum and population dynamics in space, showing that the spatial distribution of abundance may be related to life history characteristics.     

Pushed to the edge: Spatial sorting can slow down invasions

Our ability to understand population spread dynamics is complicated by rapid evolution, which renders simple ecological models insufficient. If dispersal ability evolves, more highly dispersive individuals may arrive at the population edge than less dispersive individuals (spatial sorting), accelerating spread. If individuals at the low-density population edge benefit (escape competition), high dispersers have a selective advantage (spatial selection). These two processes are often described as forming a positive feedback loop; they reinforce each other, leading to faster spread. Although spatial sorting is close to universal, this form of spatial selection is not: low densities can be detrimental for organisms with Allee effects. Here, we present two conceptual models to explore the feedback loops that form between spatial sorting and spatial selection. We show that the presence of an Allee effect can reverse the positive feedback loop between spatial sorting and spatial selection, creating a negative feedback loop that slows population spread.     

Variation between individuals fosters regional species coexistence

Although individual‐level variation (IV) is ubiquitous in nature, it is not clear how it influences species coexistence. Theory predicts that IV will hinder coexistence but empirical studies have shown that it can facilitate, inhibit, or have a neutral effect. We use a theoretical model to explore the consequences of IV on local and regional species coexistence in the context of spatial environmental structure. Our results show that individual variation can have a positive effect on species coexistence and that this effect will critically depend on the spatial structure of such variation. IV facilitates coexistence when a negative, concave‐up relationship between individuals’ competitive response and population growth rates propagates to a disproportionate advantage for the inferior competitor, provided that each species specialises in a habitat. While greater variation in the preferred habitat generally fosters coexistence, the opposite is true for non‐preferred habitats. Our results reconcile theory with empirical findings.     

Density-dependent dispersal in host-parasitoid assemblages

Most spatial population models assume constant rates of dispersal. However, in a given community, dispersal may not only depend on the density of conspecifics, i.e. density‐dependent dispersal, but also on the density of other species, a phenomenon we term ‘community‐dependent dispersal’. We co‐vary the densities of both the beetle host Callosobruchus chinensis and its parasitoid wasp, Anisopteromalus calandrae, in a laboratory study and record the proportions of each species that disperse within a two‐hour period. The parasitoid in these systems exhibits community‐dependent dispersal – dispersing more frequently when parasitoid density is high and larval host density is low. This supported our prediction that individuals should disperse according to competition for available resources. However, in this study the host's dispersal was independent of density. We suggest that this may be due to less intense selection acting on host dispersal strategies than on the parasitoid. We consider some possible consequences of community‐dependent dispersal for a number of spatial population processes. A well‐known host‐parasitoid metapopulation model is expanded so that it includes a greater range of dispersal functions. When the model is parameterised with the parasitoid community‐dependent dispersal function observed in the empirical study, similar population dynamics are obtained as when fixed‐rate dispersal functions are applied. The importance of dispersal functions for invasions of both competitive and host‐parasitoid systems is also considered. The model results demonstrate that understanding how individuals disperse in response to different species’ population densities is important in determining the rate of spread of an invasion. We suggest that more empirical studies are needed to establish what determines dispersal rate and distance in a range of species, combined with theoretical studies investigating the role of the dispersal function in determining spatial population processes.