Joint evolution of sex ratio and dispersal: conditions for higher dispersal rates from good habitats

We analyze models of evolution of sex ratio conditional on habitat quality and with sex specific dispersal. Previous analysis concluded that the main constraint on sex ratio is habitat choice and leads to overproduction of the most dispersing sex in low quality habitat. Here, we analyze three models with finite local populations and show that constraints on sex ratio can balance constraints on habitat choice. In the first model, dispersal rates are fixed. In the second, sex specific dispersal can evolve independently of the habitat quality. These models suggests that sex ratio evolution can lead to higher global dispersal rates (mean of male and female dispersal rates) from high quality habitats. In the last model dispersal evolves conditionally with both sex and habitat. Our models suggests that conditions for overproduction of the most dispersing sex in high quality habitat are frequent. The predictions of the models with evolving dispersal contrast with patterns generally described in nature. We discuss possible reasons of this difference.     

ASYMMETRIC PATCH SIZE DISTRIBUTION LEADS TO DISRUPTIVE SELECTION ON DISPERSAL

Numerous models have been designed to understand how dispersal ability evolves when organisms live in a fragmented landscape. Most of them predict a single dispersal rate at evolutionary equilibrium, and when diversification of dispersal rates has been predicted, it occurs as a response to perturbation or environmental fluctuation regimes. Yet abundant variation in dispersal ability is observed in natural populations and communities, even in relatively stable environments. We show that this diversification can operate in a simple island model without temporal variability: disruptive selection on dispersal occurs when the environment consists of many small and few large patches, a common feature in natural spatial systems. This heterogeneity in patch size results in a high variability in the number of related patch mates by individual, which, in turn, triggers disruptive selection through a high per capita variance of inclusive fitness. Our study provides a likely, parsimonious and testable explanation for the diversity of dispersal rates encountered in nature. It also suggests that biological conservation policies aiming at preserving ecological communities should strive to keep the distribution of patch size sufficiently asymmetric and variable.     

Joint evolution of differential seed dispersal and self‐fertilization

Differential seed dispersal, in which selfed and outcrossed seeds possess different dispersal propensities, represents a potentially important individual‐level association. A variety of traits can mediate differential seed dispersal, including inflorescence and seed size variation. However, how natural selection shapes such associations is poorly known. Here, we developed theoretical models for the evolution of mating system and differential seed dispersal in metapopulations, incorporating heterogeneous pollination, dispersal cost, cost of outcrossing and environment‐dependent inbreeding depression. We considered three models. In the ‘fixed dispersal model’, only selfing rate is allowed to evolve. In the ‘fixed selfing model’, in which selfing is fixed but differential seed dispersal can evolve, we showed that natural selection favours a higher, equal or lower dispersal rate for selfed seeds to that for outcrossed seeds. However, in the ‘joint evolution model’, in which selfing and dispersal can evolve together, evolution necessarily leads to higher or equal dispersal rate for selfed seeds compared to that for outcrossed. Further comparison revealed that outcrossed seed dispersal is selected against by the evolution of mixed mating or selfing, whereas the evolution of selfed seed dispersal undergoes independent processes. We discuss the adaptive significance and constraints for mating system/dispersal association.     

Joint evolution of specialization and dispersal in structured metapopulations

We study the joint evolution of dispersal and specialization concerning resource usage in a mechanistically underpinned structured discrete-time metapopulation model. We show that dispersal significantly affects the evolution of specialization and that specialization is a key factor that determines the possibility of evolutionary branching in dispersal propensity. Allowing both dispersal propensity and specialization to evolve as a consequence of natural selection is necessary in order to understand the evolutionary dynamics. The joint evolution of dispersal and specialization forms a natural evolutionary path leading to the coexistence of generalists and specialists. We show that in this process, the number of different patch types and the resource distribution are essential.     

Competition between relatives and the evolution of dispersal in a parasitoid wasp

Evolutionary theory predicts that levels of dispersal vary in response to the extent of local competition for resources and the relatedness between potential competitors. Here, we test these predictions by making use of a female dispersal dimorphism in the parasitoid wasp Melittobia australica. We show that there are two distinct female morphs, which differ in morphology, pattern of egg production, and dispersal behaviour. As predicted by theory, we found that greater competition for resources resulted in increased production of dispersing females. In contrast, we did not find support for the prediction that high relatedness between competitors increases the production of dispersing females in Melittobia. Finally, we exploit the close links between the evolutionary processes leading to selection for dispersal and for biased sex ratios to examine whether the pattern of dispersal can help distinguish between competing hypotheses for the lack of sex ratio adjustment in Melittobia.     

The social evolution of dispersal with public goods cooperation

Selection can favour the evolution of individually costly dispersal if this alleviates competition between relatives. However, conditions that favour altruistic dispersal also mediate selection for other social behaviours, such as public goods cooperation, which in turn is likely to mediate dispersal evolution. Here, we investigate – both experimentally (using bacteria) and theoretically – how social habitat heterogeneity (i.e. the distribution of public goods cooperators and cheats) affects the evolution of dispersal. In addition to recovering the well‐known theoretical result that the optimal level of dispersal increases with genetic relatedness of patch mates, we find both mathematically and experimentally that dispersal is always favoured when average patch occupancy is low, but when average patch occupancy is high, the presence of public goods cheats greatly alters selection for dispersal. Specifically, when public goods cheats are localized to the home patch, higher dispersal rates are favoured, but when cheats are present throughout available patches, lower dispersal rates are favoured. These results highlight the importance of other social traits in driving dispersal evolution.     

The evolution of environmental and genetic sex determination in fluctuating environments

Twenty years ago, Bulmer and Bull suggested that disruptive selection, produced by environmental fluctuations, can result in an evolutionary transition from environmental sex determination (ESD) to genetic sex determination (GSD). We investigated the feasibility of such a process, using mutation-limited adaptive dynamics and individual-based computer simulations. Our model describes the evolution of a reaction norm for sex determination in a metapopulation setting with partial migration and variation in an environmental variable both within and between local patches. The reaction norm represents the probability of becoming a female as a function of environmental state and was modeled as a sigmoid function with two parameters, one giving the location (i.e., the value of the environmental variable for which an individual has equal chance of becoming either sex) and the other giving the slope of the reaction norm for that environment. The slope can be interpreted as being set by the level of developmental noise in morph determination, with less noise giving a steeper slope and a more switchlike reaction norm. We found convergence stable reaction norms with intermediate to large amounts of developmental noise for conditions characterized by low migration rates, small differential competitive advantages between the sexes over environments, and little variation between individual environments within patches compared to variation between patches. We also considered reaction norms with the slope parameter constrained to a high value, corresponding to little developmental noise. For these we found evolutionary branching in the location parameter and a transition from ESD toward GSD, analogous to the original analysis by Bulmer and Bull. Further evolutionary change, including dominance evolution, produced a polymorphism acting as a GSD system with heterogamety. Our results point to the role of developmental noise in the evolution of sex determination.     

The relative influence of density and kinship on dispersal in the common lizard

We experimentally investigated the relative role of kinshipand density on juvenile dispersal in the common lizard. A fewdays after birth, juveniles were introduced into seminaturalendosures, where they experienced different social environmentsin the first experiment we varied the density of unrelated adults(males or females) within the enclosure (0, 1, or 2 adults),and in the second experiment, we varied the level of kinshipand familiarity between juveniles and adults. Each enclosurewas connected to a second enclosure by small holes which allowedonly juveniles to move between enclosures. Juvenile movementswere monitored during 14 days after birth, as juvenile dispersalis mainly completed within 10 days after birth under naturalconditions. Most juveniles did not return to the first enclosure.Sex had no effect on juvenile dispersal. Adult densityand kinshipwith adults both affected dispersal. Adult female density increasedjuvenile dispersal whatever the level of kinship and familiaritywith the females. Dispersers had better body condition thannondispersers at high female densit and this difference wassignificantly greater when the mother and the familiar femalewere present in the enclosure. Furthermore, body condition ofmothers and familiar females was positively correlated withjuvenile dispersal, whereas there was no such correlation inthe case of unfamiliar and unrelated females. These resultsstrongly suggest that adult female density is a major factorpromoting dispersal in this species and that both intraspecificand kin competition motivate dispersal.     

The sex chromosome system can influence the evolution of sex‐biased dispersal

Sex‐biased dispersal is a much‐discussed feature in literature on dispersal. Diverse hypotheses have been proposed to explain the evolution of sex‐biased dispersal, a difference in dispersal rate or dispersal distance between males and females. An early hypothesis has indicated that it may rely on the difference in sex chromosomes between males and females. However, this proposal was quickly rejected without a real assessment. We propose a new perspective on this hypothesis by investigating the evolution of sex‐biased dispersal when dispersal genes are sex‐linked, that is when they are located on the sex chromosomes. We show that individuals of the heterogametic sex disperse relatively more than do individuals of the homogametic sex when dispersal genes are sex‐linked rather than autosomal. Although such a sex‐biased dispersal towards the heterogametic sex is always observed in monogamous species, the mating system and the location of dispersal genes interact to modulate sex‐biased dispersal in monandry and polyandry. In the context of the multicausality of dispersal, we suggest that sex‐linked dispersal genes can influence the evolution of sex‐biased dispersal.     

Transmission,relatedness, and the evolution of cooperative symbionts

Cooperative interactions between species, termed mutualisms, play a key role in shaping natural ecosystems, economically important agricultural systems, and in influencing human health. Across different mutualisms, there is significant variation in the benefit that hosts receive from their symbionts. Empirical data suggest that transmission mode can help explain this variation: vertical transmission, where symbionts infect their host's offspring, leads to symbionts that provide greater benefits to their hosts than horizontal transmission, where symbionts leave their host and infect other hosts in the population. However, two different theoretical explanations have been given for this pattern: firstly, vertical transmission aligns the fitness interests of hosts and their symbionts; secondly, vertical transmission leads to increased relatedness between symbionts sharing a host, favouring cooperation between symbionts. We used a combination of analytical models and dynamic simulations to tease these factors apart, in order to compare their separate influences and see how they interact. We found that relatedness between symbionts sharing a host, rather than transmission mode per se, was the most important factor driving symbiont cooperation. Transmission mode mattered mainly because it determined relatedness. We also found evolutionary branching throughout much of our simulation, suggesting that a combination of transmission mode and multiplicity of infections could lead to the stable coexistence of different symbiont strategies.     

Kin competition,natal dispersal and the moulding of senescence by natural selection

Most theoretical models for the evolution of senescence have assumed a very large, well mixed population. Here, we investigate how limited dispersal and kin competition might influence the evolution of ageing by deriving indicators of the force of selection, similar to Hamilton (Hamilton 1966 J. Theor. Biol. 12, 12–45). Our analytical model describes how the strength of selection on survival and fecundity changes with age in a patchy population, where adults are territorial and a fraction of juveniles disperse between territories. Both parent–offspring competition and sib competition then affect selection on age-specific life-history traits. Kin competition reduces the strength of selection on survival. Mutations increasing mortality in some age classes can even be favoured by selection, but only when fecundity deteriorates rapidly with age. Population structure arising from limited dispersal however selects for a broader distribution of reproduction over the lifetime, potentially slowing down reproductive senescence. The antagonistic effects of limited dispersal on age schedules of fecundity and mortality cast doubts on the generality of conditions allowing the evolution of ‘suicide genes’ that increase mortality rates without other direct pleiotropic effects. More generally, our model illustrates how limited dispersal and social interactions can indirectly produce patterns of antagonistic pleiotropy affecting vital rates at different ages.     

The long-term evolution of multilocus traits under frequency-dependent disruptive selection

Frequency-dependent disruptive selection is widely recognized as an important source of genetic variation. Its evolutionary consequences have been extensively studied using phenotypic evolutionary models, based on quantitative genetics, game theory, or adaptive dynamics. However, the genetic assumptions underlying these approaches are highly idealized and, even worse, predict different consequences of frequency-dependent disruptive selection. Population genetic models, by contrast, enable genotypic evolutionary models, but traditionally assume constant fitness values. Only a minority of these models thus addresses frequency-dependent selection, and only a few of these do so in a multilocus context. An inherent limitation of these remaining studies is that they only investigate the short-term maintenance of genetic variation. Consequently, the long-term evolution of multilocus characters under frequency-dependent disruptive selection remains poorly understood. We aim to bridge this gap between phenotypic and genotypic models by studying a multilocus version of Levene's soft-selection model. Individual-based simulations and deterministic approximations based on adaptive dynamics theory provide insights into the underlying evolutionary dynamics. Our analysis uncovers a general pattern of polymorphism formation and collapse, likely to apply to a wide variety of genetic systems: after convergence to a fitness minimum and the subsequent establishment of genetic polymorphism at multiple loci, genetic variation becomes increasingly concentrated on a few loci, until eventually only a single polymorphic locus remains. This evolutionary process combines features observed in quantitative genetics and adaptive dynamics models, and it can be explained as a consequence of changes in the selection regime that are inherent to frequency-dependent disruptive selection. Our findings demonstrate that the potential of frequency-dependent disruptive selection to maintain polygenic variation is considerably smaller than previously expected.     

On the evolution of dispersal via heterogeneity in spatial connectivity

Dispersal has long been recognized as a mechanism that shapes many observed ecological and evolutionary processes. Thus, understanding the factors that promote its evolution remains a major goal in evolutionary ecology. Landscape connectivity may mediate the trade-off between the forces in favour of dispersal propensity (e.g. kin-competition, local extinction probability) and those against it (e.g. energetic or survival costs of dispersal). It remains, however, an open question how differing degrees of landscape connectivity may select for different dispersal strategies. We implemented an individual-based model to study the evolution of dispersal on landscapes that differed in the variance of connectivity across patches ranging from networks with all patches equally connected to highly heterogeneous networks. The parthenogenetic individuals dispersed based on a flexible logistic function of local abundance. Our results suggest, all else being equal, that landscapes differing in their connectivity patterns will select for different dispersal strategies and that these strategies confer a long-term fitness advantage to individuals at the regional scale. The strength of the selection will, however, vary across network types, being stronger on heterogeneous landscapes compared with the ones where all patches have equal connectivity. Our findings highlight how landscape connectivity can determine the evolution of dispersal strategies, which in turn affects how we think about important ecological dynamics such as metapopulation persistence and range expansion.     

Evolution of condition-dependent dispersal under kin competition

Dispersers often differ in body condition from non-dispersers. The social dominance hypothesis explains dispersal of weak individuals, but it is not yet well understood why strong individuals, which could easily retain their natal site, are sometimes exposed to risky dispersal. Based on the model for dispersal under kin competition by Hamilton and May, we construct a model where dispersal propensity depends on body condition. We consider an annual species that inhabits a patchy environment with varying patch qualities. Offspring body condition corresponds to the quality of the natal patch and competitive ability increases with body condition. Our main general result balances the fitness benefit from not dispersing and retaining the natal patch and the benefit from dispersing and establishing somewhere else. We present four different examples for competition, which all hint that dispersal of strong individuals may be a common outcome under the assumptions of the present model. In three of the examples, the evolutionarily stable dispersal probability is an increasing function of body condition. However, we found an example where, counterintuitively, the evolutionarily stable dispersal probability is a non-monotone function of body condition such that both very weak and very strong individuals disperse with high probability but individuals of intermediate body condition do not disperse at all.     

Emergence of asymmetry in evolution

We investigate symmetry-breaking bifurcation patterns in evolution in the framework of adaptive dynamics (AD). We define weak and strong symmetry. The former applies for populations where only the simultaneous reflection of all individuals is an invariant transformation. The symmetry is strong in populations where reflection of some, but not all, individuals leaves the situation unchanged. We show that in case of weak symmetry evolutionary branching can lead to the emergence of two asymmetric variants, which are mirror images of each other, and the loss of the symmetric ancestor. We also show that in case of strong symmetry, evolutionary branching can occur into a symmetric and an asymmetric variant, both of which survive. The latter, asymmetric branching differs from the generic branching patterns of AD, which is always symmetric. We discuss biological examples for weak and strong symmetries and a specific model producing the new kind of branching.     

Divergent evolution of dispersal in a heterogeneous landscape

The evolution of dispersal is investigated in a landscape of many patches with fluctuating carrying capacities and spatial heterogeneity in temporal fluctuations. Although asynchronous temporal fluctuations select for dispersal, spatial heterogeneity in the distribution of fluctuating environmental variables selects against it. We find evolutionary branching in dispersal rate leading to the evolutionarily stable coexistence of a high- and a low-dispersal phenotype. We study how the opposing forces of selection for and against dispersal change with the relative size and the environmental qualities of the source and sink habitats. Our results suggest that the evolution of dispersal dimorphism could be a first step towards speciation and local adaptation.     

Mother-offspring interactions do not affect natal dispersal in a small rodent

According to kin selection and inbreeding avoidance hypotheses,natal dispersal should be facultatively adjusted to balancingthe costs and benefits of mother–offspring interactions.In polygynous mammals, it is hypothesized that female offspringshould seek to avoid local resource competition with their mother,whereas male dispersal should be determined by inbreeding avoidance.We tested these hypotheses with a field experiment investigatingthe relationship between territory acquisition and mother'spresence in the root vole Microtus oeconomus. This species hasa flexible social system in which sisters' and mother's homeranges overlap substantially, whereas sons disperse to a greaterextent. Immature sibling voles aged 20 days were released for20 days together with an unrelated adult male in a 2-patch systemeither in the presence of their mother or in the presence ofan unrelated adult female. Offspring movements were not influencedby mother's presence, but offspring, especially females, avoidedthe patch occupied by the adult female irrespective of kinship.Offspring remaining in contact with their mother were reproductivelysuppressed at the middle, but not by the end, of the experimentalperiod. These results indicate that juvenile root voles adoptedan opportunistic settlement strategy where they avoided theadult female irrespective of kinship and inbreeding risks.     

Evolution of body condition‐dependent dispersal in metapopulations

Body condition‐dependent dispersal strategies are common in nature. Although it is obvious that environmental constraints may induce a positive relationship between body condition and dispersal, it is not clear whether positive body conditional dispersal strategies may evolve as a strategy in metapopulations. We have developed an individual‐based simulation model to investigate how body condition–dispersal reaction norms evolve in metapopulations that are characterized by different levels of environmental stochasticity and dispersal mortality. In the model, body condition is related to fecundity and determined either by environmental conditions during juvenile development (adult dispersal) or by those experienced by the mother (natal dispersal). Evolutionarily stable reaction norms strongly depend on metapopulation conditions: positive body condition dependency of dispersal evolved in metapopulation conditions with low levels of dispersal mortality and high levels of environmental stochasticity. Negative body condition‐dependent dispersal evolved in metapopulations with high dispersal mortality and low environmental stochasticity. The latter strategy is responsible for higher dispersal rates under kin competition when dispersal decisions are based on body condition reached at the adult life stage. The evolution of both positive and negative body condition‐dependent dispersal strategies is consequently likely in metapopulations and depends on the prevalent environmental conditions.     

Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister-sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that 'family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism'.     

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.