Sex biases in dispersal and philopatry: insights from a meta-analysis based on capture–mark–recapture studies of damselflies

Sex-biased dispersal is well known for birds and mammals, typically by females and males, respectively. Little is known about general patterns of sex-biased dispersal in other animal taxa. We reviewed return rates for a model group of invertebrates (damselflies) and explored putative costs and benefits of dispersal by males and females. We used published capture–mark–recapture data and examined whether a sex bias existed in likelihood of recapture at least once, at both emergence and/or breeding sites. We assessed whether this metric of likelihood of recapture was indicative of dispersal or philopatry, and whether any emerging pattern(s) were consistent across damselfly families. Using a meta-analysis, we found a higher likelihood of recapture at least once for males than for females at both natal sites and breeding sites, which seemed attributable to higher female-biased dispersal, although female-biased mortality cannot be discounted particularly for some species. Sex biases in dispersal among damselflies may be understood based on sex differences in maturation rate and foraging behaviour, both of which should affect the costs and benefits of dispersing. This hypothesis may be useful for explaining patterns of dispersal in other animal taxa.     

Genetic spatial autocorrelation can readily detect sex-biased dispersal

Sex-biased dispersal is expected to generate differences in the fine-scale genetic structure of males and females. Therefore, spatial analyses of multilocus genotypes may offer a powerful approach for detecting sex-biased dispersal in natural populations. However, the effects of sex-biased dispersal on fine-scale genetic structure have not been explored. We used simulations and multilocus spatial autocorrelation analysis to investigate how sex-biased dispersal influences fine-scale genetic structure. We evaluated three statistical tests for detecting sex-biased dispersal: bootstrap confidence intervals about autocorrelation r values and recently developed heterogeneity tests at the distance class and whole correlogram levels. Even modest sex bias in dispersal resulted in significantly different fine-scale spatial autocorrelation patterns between the sexes. This was particularly evident when dispersal was strongly restricted in the less-dispersing sex (mean distance <200 m), when differences between the sexes were readily detected over short distances. All tests had high power to detect sex-biased dispersal with large sample sizes (n ≥ 250). However, there was variation in type I error rates among the tests, for which we offer specific recommendations. We found congruence between simulation predictions and empirical data from the agile antechinus, a species that exhibits male-biased dispersal, confirming the power of individual-based genetic analysis to provide insights into asymmetries in male and female dispersal. Our key recommendations for using multilocus spatial autocorrelation analyses to test for sex-biased dispersal are: (i) maximize sample size, not locus number; (ii) concentrate sampling within the scale of positive structure; (iii) evaluate several distance class sizes; (iv) use appropriate methods when combining data from multiple populations; (v) compare the appropriate groups of individuals.     

Sex ratio evolution when fitness and dispersal vary

In a heterogeneous environment, when the fitness of males and females are differently influenced by habitat quality, habitat-dependent sex ratios may evolve to favor the production of the sex that benefits more (or loses less) from the local habitat. Similarly, sex-biased dispersal favors the evolution of habitat-dependent sex ratios. The present study documents the convergence stable sex ratios expected in the presence of sex-specific fitness gains when dispersal is partial, sex-biased or costly, using a simple model with patches of two qualities. Results show that partial dispersal reduces the sex ratio bias expected with sex-specific fitness gains. The direction of the sex ratio bias can be reversed by sex-biased dispersal or the existence of sex-specific dispersal costs, provided that fitness gains for the two sexes are not too different. The reversal of the sex ratio bias is more readily observed when sex-specific dispersal rates are opposite and extreme. Both dispersal and fitness gains, especially when they are sex-specific, should thus be considered when making predictions about sex ratio evolution in a heterogeneous environment.     

A spatially explicit model of sex ratio evolution in response to sex-biased dispersal

Sex-biased dispersal occurs in all seed plants and many animal species. Theoretical models have shown that sex-biased dispersal can lead to evolutionarily stable biased sex ratios. Here, we use a spatially explicit chessboard model to simulate the evolution of sex ratio in response to sex-biased dispersal range and sex-biased dispersal rate. Two life cycles are represented in the model: one in which both sexes disperse before mating (DDM), the other in which males disperse before mating and mated females or zygotes disperse after mating (DMD). Model parameters include factors like dispersal rate, dispersal range, number of individuals per patch, and habitat heterogeneity.When dispersal range is sex biased, we find that, in a homogeneous environment, the sex ratio is generally biased towards the sex that disperses more widely (sex ratio range: 0.47–0.52). In a heterogeneous environment, the sex ratio is generally biased towards the more dispersive sex in good habitats, and towards the less dispersive sex in poor habitats (sex ratio range: 0–1). This is opposite to the effect of sex-biased dispersal rate, which favours the production of the more dispersive sex in poor habitats and the less dispersive sex in good habitats (sex ratio range: 0–1). To allow for a comparison with theoretical predictions, data concerning sex-biased dispersal and habitat-dependent sex ratios should thus incorporate information about the spatial scale of both dispersal and environmental heterogeneity.     

Fine scale relationships between sex, life history, and dispersal of masu salmon

Identifying the patterns and processes driving dispersal is critical for understanding population structure and dynamics. In many organisms, sex-biased dispersal is related to the type of mating system. Considerably, less is known about the influence of life-history variability on dispersal. Here we investigated patterns of dispersal in masu salmon (Oncorhynchus masou) to evaluate influences of sex and life history on dispersal. As expected, assignment tests and isolation by distance analysis revealed that dispersal of marine-migratory masu salmon was male-biased. However, dispersal of resident and migratory males did not follow our expectation and marine-migratory individuals dispersed more than residents. This may be because direct competition between marine-migratory and resident males is weak or that the cost of dispersal is smaller for marine-migratory individuals. This study revealed that both sex and migratory life-history influence patterns of dispersal at a local scale in masu salmon.     

Sex-biased dispersal and inbreeding avoidance in birds and mammals

Sex differences in dispersal distance are widespread in birds and mammals, but the predominantly dispersing sex differs consistently between the classes. There has been persistent debate over the relative importance of two factors - intrasexual competition and inbreeding avoidance - in producing sex-biased dispersal, and over the sources of the difference in dispersal patterns between the two classes. Recent studies cast new light on these questions.     

Microsatellite data show evidence for male-biased dispersal in the Caribbean lizard Anolis roquet

Dispersal is a key component of an organism's life history and differences in dispersal between sexes appear to be widespread in vertebrates. However, most predictions of sex-biased dispersal have been based on observations of social structure in birds and mammals and more data are needed on other taxa to test whether these predictions apply in other organisms. Caribbean anole lizards are important model organisms in various biological disciplines, including evolutionary biology. However, very little is known about their dispersal strategies despite the importance of dispersal for population structure and dynamics. Here we use nine microsatellite markers to assess signatures of sex-biased dispersal on two spatial sampling scales in Anolis roquet, an anole endemic to the island of Martinique. Significantly higher gene diversity (H(S)) and lower mean assignment value (mAIC) was found in males on the larger spatial sampling scale. Significant heterozygote deficit (F(IS)), lower population differentiation (F(ST)), mAIC and variance of assignment index (vAIC) was found in males on the smaller spatial scale. The observation of male biased dispersal conform with expectations based on the polygynous mating system of Anolis roquet, and contributes to an explanation of the contrasting patterns of genetic structure between maternal and biparental markers that have been reported previously in this, and other anoline, species.     

Does social complexity lead to sex-biased dispersal in polygynous mammals? A test on ground-dwelling sciurids

Mating systems are well known to influence the dispersing sex,but the magnitude of the sex-biased dispersal has not actuallybeen measured, whereas many theoretical predictions have beenmade. In this study, we tested a new prediction about the coevolutionbetween natal dispersal and sociality from a recent evolutionarilystable strategy (ESS) approach. From a comparative approach,we showed that, in agreement with the model, the male-biaseddispersal increases with increasing level of sociality in polygynousground-dwelling sciurids. In addition, the increase in male-biaseddispersal with increasing sociality results from an increasein male dispersal rates, whereas female dispersal rates remainconstant, contrary to what is expected from the ESS model. Althoughthe mating system through the level of polygyny could act asa confounding factor, our results strengthen previous work thatstates that inbreeding avoidance plays a major role in the evolutionof dispersal for the most social mammalian species.     

Fine-scale population differentiation and gene flow in a terrestrial salamander (Plethodon cinereus) living in continuous habitat

Several recent studies have shown that amphibian populations may exhibit high genetic subdivision in areas with recent fragmentation and urban development. Less is known about the potential for genetic differentiation in continuous habitats. We studied genetic differentiation of red-backed salamanders (Plethodon cinereus) across a 2-km transect through continuous forest in Virginia, USA. Mark-recapture studies suggest very little dispersal for this species, whereas homing experiments and post-Pleistocene range expansion both suggest greater dispersal abilities. We used six microsatellite loci to examine genetic population structure and differentiation between eight subpopulations of red-backed salamanders at distances from 200 m to 2 km. We also used several methods to extrapolate dispersal frequencies and test for sex-biased dispersal. We found small, but detectable differentiation among populations, even at distances as small as 200 m. Differentiation was closely correlated with distance and both Mantel tests and assignment tests were consistent with an isolation-by-distance model for the population. Extrapolations of intergenerational variance in spatial position (sigma(2)<15 m(2)) and pair-wise dispersal frequencies (4 Nm < 25 for plots separated by 300 m) both suggest limited gene flow. Additionally, tests for sex-biased dispersal imply that dispersal frequency is similarly low for both sexes. We suggest that these low levels of gene flow and the infrequent dispersal observed in mark-recapture studies may be reconciled with homing ability and range expansion if dispersing animals rarely succeed in breeding in saturated habitats, if dispersal is flexible depending on the availability of habitat, or if dispersal frequency varies across the geographic range of red-backed salamanders.     

Fluctuating sex ratios,but no sex-biased dispersal,in a promiscuous fish

Dispersal in birds and mammals tends to be female-biased in monogamous species and male-biased in polygamous species. However results for other taxa, most notably fish, are equivocal. We employed molecular markers and physical tags to test the hypothesis that Atlantic salmon, a promiscuous species with intense male-male competition for access to females, displays male-biased dispersal. We found significant variation in sex ratios and in asymmetric gene flow between neighbouring salmon populations, but little or no evidence for sex-biased dispersal. We show that conditions favouring male dispersal will often be offset by those favouring female dispersal, and that spatial and temporal variation in sex ratios within a metapopulation may favour the dispersal of different sexes in source and sink habitats. Thus, our results reconcile previous discrepancies on salmonid dispersal and highlight the need to consider metapopulation dynamics and sex ratios in the study of natal dispersal of highly fecund species.     

Sex-biased survival and philopatry in birds: Do they interact?

A review of studies of sex-biased dispersal and philopatry and sex-biased survival in birds is presented. The comparison between sex-related mortality and natal and breeding dispersal at the species-level shows that dispersing birds (mainly females) suffer higher mortality, while philopatric birds (mainly males) have higher survival. The interaction between sex-biased survival and spatial behavior is a crucial component of avian vital strategy, which determine population dynamics and genetic structure.     

Using Genealogical Mapping and Genetic Neighborhood Sizes to Quantify Dispersal Distances in the Neotropical Passerine,the Black-Capped Vireo

Dispersal is a key demographic process, ultimately responsible for genetic connectivity among populations. Despite its importance, quantifying dispersal within and between populations has proven difficult for many taxa. Even in passerines, which are among the most intensely studied, individual movement and its relation to gene flow remains poorly understood. In this study we used two parallel genetic approaches to quantify natal dispersal distances in a Neotropical migratory passerine, the black-capped vireo. First, we employed a strategy of sampling evenly across the landscape coupled with parentage assignment to map the genealogical relationships of individuals across the landscape, and estimate dispersal distances; next, we calculated Wright’s neighborhood size to estimate gene dispersal distances. We found that a high percentage of captured individuals were assigned at short distances within the natal population, and males were assigned to the natal population more often than females, confirming sex-biased dispersal. Parentage-based dispersal estimates averaged 2400m, whereas gene dispersal estimates indicated dispersal distances ranging from 1600–4200 m. Our study was successful in quantifying natal dispersal distances, linking individual movement to gene dispersal distances, while also providing a detailed look into the dispersal biology of Neotropical passerines. The high-resolution information was obtained with much reduced effort (sampling only 20% of breeding population) compared to mark-resight approaches, demonstrating the potential applicability of parentage-based approaches for quantifying dispersal in other vagile passerine species.     

Mitochondrial DNA paradox: sex-specific genetic structure in a marine mussel - despite maternal inheritance and passive dispersal

ABSTRACT: BACKGROUND: When genetic structure is identified using mitochondrial DNA (mtDNA), but no structure is identified using biparentally-inherited nuclear DNA, the discordance is often attributed to differences in dispersal potential between the sexes. RESULTS: We sampled the intertidal rocky shore mussel Perna perna in a South African bay and along the nearby open coast, and sequenced maternally-inherited mtDNA (there is no evidence for paternally-inherited mtDNA in this species) and a biparentally-inherited marker. By treating males and females as different populations, we identified significant genetic structure on the basis of mtDNA data in the females only. CONCLUSIONS: This is the first study to report sex-specific differences in genetic structure based on matrilineally-inherited mtDNA in a passively dispersing species that lacks social structure or sexual dimorphism. The observed pattern most likely stems from females being more vulnerable to selection in habitats from which they did not originate, which also manifests itself in a male-biased sex ratio. Our results have three important implications for the interpretation of population genetic data. First, even when mtDNA is inherited exclusively in the female line, it also contains information about males. For that reason, using it to identify sex-specific differences in genetic structure by contrasting it with biparentally-inherited markers is problematic. Second, the fact that sex-specific differences were found in a passively dispersing species in which sex-biased dispersal is unlikely highlights the fact that significant genetic structure is not necessarily a function of low dispersal potential or physical barriers. Third, even though mtDNA is typically used to study historical demographic processes, it also contains information about contemporary processes. Higher survival rates of males in non-native habitats can erase the genetic structure present in their mothers within a single generation.     

Social Mating System and Sex-Biased Dispersal in Mammals and Birds: A Phylogenetic Analysis

The hypothesis that patterns of sex-biased dispersal are related to social mating system in mammals and birds has gained widespread acceptance over the past 30 years. However, two major complications have obscured the relationship between these two behaviors: 1) dispersal frequency and dispersal distance, which measure different aspects of the dispersal process, have often been confounded, and 2) the relationship between mating system and sex-biased dispersal in these vertebrate groups has not been examined using modern phylogenetic comparative methods. Here, we present a phylogenetic analysis of the relationship between mating system and sex-biased dispersal in mammals and birds. Results indicate that the evolution of female-biased dispersal in mammals may be more likely on monogamous branches of the phylogeny, and that females may disperse farther than males in socially monogamous mammalian species. However, we found no support for a relationship between social mating system and sex-biased dispersal in birds when the effects of phylogeny are taken into consideration. We caution that although there are larger-scale behavioral differences in mating system and sex-biased dispersal between mammals and birds, mating system and sex-biased dispersal are far from perfectly associated within these taxa.     

Highly asymmetric fine-scale genetic structure between sexes of African striped mice and indication for condition dependent alternative male dispersal tactics

Sex-biased dispersal is observed in many taxa, but few studies have compared sex-biased dispersal among and within populations. We addressed the magnitude and habitat dependency of sex-biased dispersal in social African striped mice by separating group-related from population-related genetic variance to understand the contribution of each sex to deme structure. As dispersal over unoccupied habitat is likely to be more costly than dispersal within a population, we predicted that individuals leaving the natal population have a lower body condition, being inferior to heavier territorial individuals. Fine-scale genetic structure was detected in both sexes. Female relatedness decreased continuously from R = 0.21 at 25 m to zero at 500 m. Maximum male relatedness R = 0.05 was constant at distances between 25 and 75 m, becoming zero at 100 m. Genetic variance (F(ST) ) among seven locations was significantly higher in females than in males, while inbreeding estimates (F(IS) ) were significantly higher in males than in females. Assignment tests estimated significantly more migrants among males, while Bayesian clustering estimated only a single genetic unit cluster for males among the seven locations. The mean body mass of migrant males (44 g) was significantly lower than for males that remained resident and thus dispersed within their sub-population (48 g). Combined, the results showed habitat-independent male-biased dispersal and high female philopatry, and suggested that body condition was more important than kinship in male dispersal decisions. We suggest that locally inferior males are important for gene flow between sub-populations. Thus, males might follow alternative dispersal tactics.     

Inferring recent migration rates from individual genotypes

We present a novel and straightforward method for estimating recent migration rates between discrete populations using multilocus genotype data. The approach builds upon a two-step sampling design, where individual genotypes are sampled before and after dispersal. We develop a model that estimates all pairwise backwards migration rates ( m_ij , the probability that an individual sampled in population i is a migrant from population j ) between a set of populations. The method is validated with simulated data and compared with the methods of BayesAss and Structure. First, we use data for an island model and then we consider more realistic data simulations for a metapopulation of the greater white-toothed shrew ( Crocidura russula ). We show that the precision and bias of estimates primarily depend upon the proportion of individuals sampled in each population. Weak sampling designs may particularly affect the quality of the coverage provided by 95% highest posterior density intervals. We further show that it is relatively insensitive to the number of loci sampled and the overall strength of genetic structure. The method can easily be extended and makes fewer assumptions about the underlying demographic and genetic processes than currently available methods. It allows backwards migration rates to be estimated across a wide range of realistic conditions.     

Fine-scale population genetic structure and sex-biased dispersal in the smooth snake (Coronella austriaca) in southern England

Human-induced alteration of natural habitats has the potential to impact on the genetic structuring of remnant populations at multiple spatial scales. Species from higher trophic levels, such as snakes, are expected to be particularly susceptible to land-use changes. We examined fine-scale population structure and looked for evidence of sex-biased dispersal in smooth snakes (Coronella austriaca), sampled from 10 heathland localities situated within a managed coniferous forest in Dorset, United Kingdom. Despite the limited distances between heathland areas (maximum <6 km), there was a small but significant structuring of populations based on eight microsatellite loci. This followed an isolation-by-distance model using both straight line and 'biological' distances between sampling sites, suggesting C. austriaca's low vagility as the causal factor, rather than closed canopy conifer forest exerting an effect as a barrier to dispersal. Within population comparisons of male and female snakes showed evidence for sex-biased dispersal, with three of four analyses finding significantly higher dispersal in males than in females. We suggest that the fine-scale spatial genetic structuring and sex-biased dispersal have important implications for the conservation of C. austriaca, and highlight the value of heathland areas within commercial conifer plantations with regards to their future management.     

Sex-biased dispersal: a result of a sex difference in breeding site availability

Sex-biased dispersal is often explained by assuming that the resource-defending sex pays greater costs of moving from a familiar area. We hypothesize that sex-biased dispersal may also be caused by a sex bias in breeding site availability. In avian resource-defense mating systems, site availability is often more constrained for females: males can choose from all vacant sites, whereas females are restricted to sites defended by males. Using data on breeding dispersal of a migratory passerine, we show that average number of available breeding options and availability of the previous year's territory was greater for males than females. The female bias in site unavailability may explain the female bias in probability of breeding dispersal because there was no sex bias in dispersal among birds with their previous year's territory available. We suggest that sex biases in the availability of breeding options may be an important factor contributing to observed variation in sex-biased dispersal patterns.     

Spatial sorting drives morphological variation in the invasive bird, Acridotheris tristis

The speed of range expansion in many invasive species is often accelerating because individuals with stronger dispersal abilities are more likely to be found at the range front. This 'spatial sorting' of strong dispersers will drive the acceleration of range expansion. In this study, we test whether the process of spatial sorting is at work in an invasive bird population (Common myna, Acridotheris tristis) in South Africa. Specifically, we sampled individuals across its invasive range and compared morphometric measurements relevant and non-relevant to the dispersal ability. Besides testing for signals of spatial sorting, we further examined the effect of environmental factors on morphological variations. Our results showed that dispersal-relevant traits are significantly correlated with distance from the range core, with strong sexual dimorphism, indicative of sex-biased dispersal. Morphological variations were significant in wing and head traits of females, suggesting females as the primary dispersing sex. In contrast, traits not related to dispersal such as those associated with foraging showed no signs of spatial sorting but were significantly affected by environmental variables such as the vegetation and the intensity of urbanisation. When taken together, our results support the role of spatial sorting in facilitating the expansion of Common myna in South Africa despite its low propensity to disperse in the native range.     

Sex-biased dispersal promotes adaptive parental effects

Background  

In heterogeneous environments, sex-biased dispersal could lead to environmental adaptive parental effects, with offspring selected to perform in the same way as the parent dispersing least, because this parent is more likely to be locally adapted. We investigate this hypothesis by simulating varying levels of sex-biased dispersal in a patchy environment. The relative advantage of a strategy involving pure maternal (or paternal) inheritance is then compared with a strategy involving classical biparental inheritance in plants and in animals.