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.     

Evidence for female-biased dispersal in the protandrous hermaphroditic Asian Seabass, Lates calcarifer

Movement of individuals influences individual reproductive success, fitness, genetic diversity and relationships among individuals within populations and gene exchange among populations. Competition between males or females for mating opportunities and/or local resources predicts a female bias in taxa with monogamous mating systems and a male-biased dispersal in polygynous species. In birds and mammals, the patterns of dispersal between sexes are well explored, while dispersal patterns in protandrous hermaphroditic fish species have not been studied. We collected 549 adult individuals of Asian seabass (Lates calcarifer) from four locations in the South China Sea. To assess the difference in patterns of dispersal between sexes, we genotyped all individuals with 18 microsatellites. Significant genetic differentiation was detected among and within sampling locations. The parameters of population structure (F(ST)), relatedness (r) and the mean assignment index (mAIC), in combination with data on tagging-recapture, supplied strong evidences for female-biased dispersal in the Asian seabass. This result contradicts our initial hypothesis of no sex difference in dispersal. We suggest that inbreeding avoidance of females, female mate choice under the condition of low mate competition among males, and male resource competition create a female-biased dispersal. The bigger body size of females may be a cause of the female-biased movement. Studies of dispersal using data from DNA markers and tagging-recapture in hermaphroditic fish species could enhance our understanding of patterns of dispersal in fish.     

Phylogeny,paraphyly and ecological adaptation of the colour and pattern in the Anolis roquet complex on Martinique

Martinique is an environmentally heterogeneous island with a complex geological history. It is occupied by a solitary anole, Anolis roquet, showing marked geographical variation in colour and other features. Phylogenetic analysis of a segment (1 kb) of the mitochondrial cytochrome b gene across the Anolis roquet series in the southern Lesser Antilles and at 63 localities of Anolis roquet in Martinique indicate that A. roquet is paraphyletic as A. extremus (Barbados) is nested within the Martinique populations. Moreover, divergent phylogenetic lineages exist within Martinique (max. 10.6% uncorrected pairwise), and these lineages are closely associated with the geological history of this complex island. However, objective quantification of the spectroradiometric analysis of hue by delta analysis, together with analysis of the colour pattern, indicate that they are primarily determined by adaptation to environmental conditions, irrespective of these phylogenetic lineages. There is remarkable convergence in hue and pattern in both extreme xeric (dark chevrons on a dull, generally grey/brown, background), and montane conditions (black reticulation and non-UV white spots on a bright, saturated green background). Moreover, parallel trends occur between Martinique and other Lesser Antillean anoles, which further argues for adaptation (increase in green saturation in montane areas and higher levels of UV on the dewlap of some Atlantic forms). As an exception, there are two specific situations where anoles from different lineages look different. These are (i). in the low-altitude regions of the northwest where the northwestern and central lineages make contact, and (ii). in the far south of the island where the southern and central lineages meet.     

Genetic evidence for female-biased dispersal and gene flow in a polygynous primate

Many models of sex-biased dispersal predict that the direction of sex-bias depends upon a species' mating system. In agreement with this, almost all polygynous mammals show male-biased dispersal whereas largely monogamous birds show female-biased dispersal (FBD). The hamadryas baboon (Papio hamadryas hamadryas) is polygynous and so dispersal is predicted to be male biased, as is found in all other baboon subspecies, but there are conflicting field data showing both female and male dispersal. Using 19 autosomal genetic markers genotyped in baboons from four Saudi Arabian populations, we found strong evidence for FBD in post-dispersal adults but not, as expected, in pre-dispersal infants and young juveniles, when we compared male and female: population structure (F(st)), inbreeding (F(is)), relatedness (r), and the mean assignment index (mAIc). Furthermore, we found evidence for female-biased gene flow as population genetic structure (F(st)), was about four times higher for the paternally inherited Y, than for either autosomal markers or for maternally inherited mtDNA. These results contradict the direction of sex-bias predicted by the mating system and show that FBD has evolved recently from an ancestral state of male-biased dispersal. We suggest that the cost-benefit balance of dispersal to males and females is tightly linked to the unique hierarchical social structure of hamadryas baboons and that dispersal and social organization have coevolved.     

Development of microsatellite markers in the St Lucia anole, Anolis luciae

Anolis lizards are important models in studies of ecology and evolution. Here we describe 13 polymorphic microsatellites for use in population screening in the St Lucia anole, Anolis luciae, that can be used as a natural replicate to Anolis roquet on Martinique to study processes involved in population differentiation and speciation. Genotyping of 32 individuals using M13 tails and FAM-labelled universal M13 primers showed that all loci were polymorphic with high genetic diversity, averaging at 16.8 alleles per locus. Genotypic frequencies conformed to Hardy-Weinberg expectations, and there were no instances of linkage disequilibrium between loci.     

Small-scale spatial genetic structure in an ant species with sex-biased dispersal

In a population of the monogynous, polyandrous ant Cataglyphis cursor , we analysed the spatial genetic structure of queens, colony fathers and workers at a microgeographical scale to infer the extent of sex-biased dispersal and to assess the impact of limited dispersal on the patterns of relatedness within the colony. To this end, four microsatellite markers were scored for the queen and an average of 26 workers from each of 35 mapped colonies. We used pair-wise kinship coefficients between all pairs of genotypes, including the reconstructed colony father genotypes (1) to test and quantify isolation by distance patterns within each sex or caste through the analysis of kinship–distance curves, and (2) to compute the average relatedness between categories of colony members. The kinship–distance curve was much steeper for colony queens than colony fathers, indicating male-biased dispersal. However, colony fathers also displayed a non-random spatial genetic structure, so that even males show some dispersal limitation at the scale of the population, which extends over less than 250 m. The degree of relatedness between the different sexes and castes of colonies was well predicted from the number of mates per queen and the inbreeding of queens, and the impact of limited dispersal was very weak at this scale of observation. We discuss the interest of kinship–distance curves to assess sex-biased dispersal on a local scale and we compare our results with large-scale analyses of genetic structure in Cataglyphis cursor and other monogynous ant species.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 465–473.     

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 natal philopatry in the diamondback terrapin, Malaclemys terrapin

Nesting ecology and population studies indicate that diamondback terrapins (Malaclemys terrapin) exhibit nest site fidelity and high habitat fidelity. However, genetic studies indicate high levels of gene flow. Because dispersal affects the genetics and population dynamics of a species, we used six highly polymorphic microsatellite markers to investigate sex-biased dispersal and natal philopatry of M. terrapin in Barnegat Bay, NJ. We compared results of spatial autocorrelation analysis, assignment methods and Wright's F(ST) estimators to a mark-recapture analysis. Mark-recapture analysis over a 4-year period indicated that most individuals have relatively small home ranges (<2 km), with mature females displaying greater home ranges than males. Goodness of fit analysis of our mark-recapture study indicated that some juvenile males were likely transient individuals moving through our study location. Mean assignment indices and first-generation migrant tests indicated that mature males were more prone to disperse than mature females, but first-generation migrant tests indicated that per capita there are more female than male dispersers. Thus, the relative importance of males and females on gene flow in terrapin populations may change in relation to population sex ratios. Spatial autocorrelation analysis indicated that mature females exhibited natal philopatry to nesting beaches, but first-generation migrant tests indicated that a small number of females failed to nest on natal beaches. Finally, we discuss the important conservation implications of male-biased dispersal and natal philopatry in the diamondback terrapin.     

Parentage-based pedigree reconstruction reveals female matrilineal clusters and male-biased dispersal in nongregarious Asian great apes, the Bornean orang-utans (Pongo pygmaeus)

Philopatry and sex-biased dispersal have a strong influence on population genetic structure, so the study of species dispersal patterns and evolutionary mechanisms shaping them are of great interest. Particularly nongregarious mammalian species present an underexplored field of study: despite their lower levels of sociality compared to group-living species, interactions among individuals do occur, providing opportunities for cryptic kin selection. Among the least gregarious primates are orang-utans (genus: Pongo), in which preferential associations among females have nevertheless been observed, but for which the presence of kin structures was so far unresolved because of the equivocal results of previous genetic studies. To clarify relatedness and dispersal patterns in orang-utans, we examined the largest longitudinal set of individuals with combined genetic, spatial and behavioural data. We found that males had significantly higher mitochondrial DNA (mtDNA) variation and more unique haplotypes, thus underscoring their different maternal ancestries compared to females. Moreover, pedigree reconstruction based on 24 highly polymorphic microsatellite markers and mtDNA haplotypes demonstrated the presence of three matrilineal clusters of generally highly related females with substantially overlapping ranges. In orang-utans and possibly other nongregarious species, comparing average biparental relatedness (r) of males and females to infer sex-biased dispersal is extremely problematic. This is because the opportunistic sampling regime frequently employed in nongregarious species, combined with overlapping space use of distinct matrilineal clusters, leads to a strong downward bias when mtDNA lineage membership is ignored. Thus, in nongregarious species, correct inferences of dispersal can only be achieved by combining several genetic approaches with detailed spatial information.     

Inferring sex-biased dispersal from population genetic tools: a review

Sex-biased dispersal, where individuals of one sex stay or return to their natal site (or group) to breed while individuals of the other sex are prone to disperse, is a wide-spread pattern in vertebrate organisms. In general, mammals exhibit male-biased dispersal whereas birds exhibit female-bias. Dispersal estimates are often difficult to obtain from direct field observations. Here we describe different methods for inferring sex-specific dispersal using population genetic tools and discuss the problems they can raise. We distinguish two types of methods: those based on bi-parental markers (eg comparison of male/female relatedness, F(st) and assignment probabilities) and those relying on the comparison between markers with different modes of inheritance (eg mtDNA markers and microsatellites). Finally, we discuss statistical problems that are encountered with these different methods (eg pseudoreplication, problems due to the comparison of distinct markers). While the genetic methods to detect sex-biased dispersal are now relatively well developed, their interpretation can prove problematic due to the confounding effects of factors such as the mating system of the species. Moreover, the relative power of these methods is not well known and requires further investigation.     

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.     

Fine-scale social and spatial genetic structure in Sitka black-tailed deer

The spatial extent of Sitka black-tailed deer (Odocoileus hemionus sitkensis) populations below the regional scale is relatively unknown, as is dispersal between populations. Here, we use noninvasive samples to genotype 221 Sitka black-tailed deer in three watersheds on Prince of Wales Island, Alaska, separated by a maximum of 44 km, using traditional and spatial genetic approaches. We find that despite geographic proximity, multiple lines of evidence suggest fine-scale genetic structure among the three study sites. The 2 most geographically distant watersheds differed significantly in genetic composition, suggesting an isolation-by-distance pattern. Within study sites, deer exhibited spatial genetic structure within a radius of 1,000 m. Based on a reduced sample of known-sex individuals, females exhibited positive spatial genetic structure within a radius of 500 m but males showed no structure. Moreover, females were more likely to be related to their 5 nearest female neighbors, regardless of distance, than were males. Evidence indicates dispersal by both sexes although it may be more common, or dispersal distances are greater, in males. Nonetheless, analysis of assignment indices and comparison of sex-specific correlograms found no evidence of sex-biased dispersal between watersheds. Patterns of spatial relatedness and connectivity suggest limited dispersal among Sitka black-tailed deer, creating genetic structure on a fine spatial scale, perhaps as small as the watershed.     

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.     

(Not) far from home: No sex bias in dispersal,but limited genetic patch size,in an endangered species,the Spotted Turtle (Clemmys guttata)

Sex-biased dispersal is common in many animals, with male-biased dispersal often found in studies of mammals and reptiles, including interpretations of spatial genetic structure, ostensibly as a result of male–male competition and a lack of male parental care. Few studies of sex-biased dispersal have been conducted in turtles, but a handful of studies, in saltwater turtles and in terrestrial turtles, have detected male-biased dispersal as expected. We tested for sex-biased dispersal in the endangered freshwater turtle, the spotted turtle (Clemmys guttata) by investigating fine-scale genetic spatial structure of males and females. We found significant spatial genetic structure in both sexes, but the patterns mimicked each other. Both males and females typically had higher than expected relatedness at distances <25 km, and in many distance classes greater than 25 km, less than expected relatedness. Similar patterns were apparent whether we used only loci in Hardy–Weinberg equilibrium (n = 7) or also included loci with potential null alleles (n = 5). We conclude that, contrary to expectations, sex-biased dispersal is not occurring in this species, possibly related to the reverse sexual dimorphism in this species, with females having brighter colors. We did, however, detect significant spatial genetic structure in males and females, separate and combined, showing philopatry within a genetic patch size of <25 km in C. guttata, which is concerning for an endangered species whose populations are often separated by distances greater than the genetic patch size.     

A comparison of techniques for assessing dispersal behaviour in gundis: revealing dispersal patterns in the absence of observed dispersal behaviour

Knowledge of the dispersal status of group members is important to understanding how sociality may have evolved within a species. I assessed the effectiveness of four techniques for elucidating dispersal behaviour in a rock-dwelling rodent ( Ctenodactylus gundi ) with small group sizes (2–10 animals): genetic parentage assignment, haplotype data and kinship analyses, assignment testing, and F -statistics. The first two methods provided the greatest insight into gundi dispersal behaviour. Assignment testing and F -statistics proved of limited use for elucidating fine-scale dispersal, but could detect large-scale patterns despite low sex-biased dispersal intensity (1.9 : 1) because of moderate genetic differentiation among groups ( F _ST = 0.10). Findings are discussed in light of current dispersal theory. In general, gundi dispersal is plastic, and seems to be dependent on body weight (for males), group composition, and scale of analysis (total dispersal events recorded within the population were almost twice the immigration rate into the population). Most groups were comprised of a single matriline and one immigrant male. Immigrant rather than philopatric males bred with group females. Dispersal among groups was male-biased, but dispersal or philopatry could occur by either sex. During a drought, both sexes delayed dispersal and cooperative social units formed. Whether such behaviour resulted directly from the drought or not remains unclear, however, since comparative information was not available from nondrought years. Combining fine-scale analyses with information on large-scale patterns provided substantial insight into gundi dispersal behaviour despite the limited movement of animals during a drought, and may prove useful for elucidating dispersal behaviour in other social animals.     

Female philopatry and male-biased dispersal in a direct-developing salamander, Plethodon cinereus

The local resource competition hypothesis and the local mate competition hypothesis were developed based on avian and mammalian systems to explain sex-biased dispersal. Most avian species show a female bias in dispersal, ostensibly due to resource defence, and most mammals show a male bias, ostensibly due to male-male competition. These findings confound phylogeny with mating strategy; little is known about sex-biased dispersal in other taxa. Resource defence and male-male competition are both intense in Plethodon cinereus, a direct-developing salamander, so we tested whether sex-biased dispersal in this amphibian is consistent with the local resource competition hypothesis (female-biased) or the local mate competition hypothesis (male-biased). Using fine-scale genetic spatial autocorrelation analyses, we found that females were philopatric, showing significant positive genetic structure in the shortest distance classes, with stronger patterns apparent when only territorial females were tested. Males showed no spatial genetic structure over the shortest distances. Mark-recapture observations of P. cinereus over 5 years were consistent with the genetic data: males dispersed farther than females during natal dispersal and 44% of females were recaptured within 1 m of their juvenile locations. We conclude that, in this population of a direct-developing amphibian, females are philopatric and dispersal is male-biased, consistent with the local mate competition hypothesis.     

Intraspecific variation in the direction and degree of sex-biased dispersal among sea-snake populations

Higher rates of dispersal in one sex than the other are widespread, and often attributed to the genetic advantages of reduced inbreeding. The direction of sex-biased dispersal shows strong phylogenetic conservatism (e.g. males disperse more than females in most mammals, but the reverse is true in most birds). By contrast, our genetic data reveal strong inter-population variation in the relative dispersal rates of two species of sea snakes (Laticauda saintgironsi and L. laticaudata) in the Noumea Lagoon of New Caledonia. Assignment methods using microsatellite data identified parallel variation in sex-specific dispersal in both species: dispersal was female-biased in the north-west of the sampling area (in islands far from the main island), but male-biased in the south-east (in islands closer to the main island). This flexibility may reflect sex differences in diets, with spatial variation in sex-specific resources generating spatial variation in sex-specific dispersal distances.     

Population differentiation and nuclear gene flow in the Dominican anole (Anolis oculatus)

Allele frequency data from nuclear microsatellite loci were used to investigate patterns of nuclear gene flow and population structure in the morphologically variable Dominican anole (Anolis oculatus). All six loci used proved to be highly polymorphic, with an average of 18.8 alleles per locus. Test for Hardy-Weinberg equilibrium revealed small numbers of heterozygote deficiencies at single loci in single populations and consistent patterns of increasingly significant heterozygote deficiency in global tests across populations and loci. No significant relationship between FST and patristic distances estimated from mitochondrial DNA sequences was detected and estimates of FIS were significantly higher in females than in males, indicating that gene flow may be sex-biased and mediated mainly by male migration. A highly significant correlation between linearized FST and loge (geographical distance) indicates that geographical proximity is a significant factor in the genetic structure of A. oculatus populations. However, levels of gene flow between morphologically differentiated parapatric populations are frequently seen to be relatively high. This supports the hypothesis of natural selection being the driving force behind the development and maintenance of morphological variation and shows that adaptive differentiation may be maintained despite the homogenizing influence of gene flow. Generally, the morphologically variable populations of A. oculatus are seen to be poor candidates for in situ speciation, but an exceptional case on the west coast of Dominica indicates that isolation resulting from vicariant events may lead to rapid differentiation at both mitochondrial and nuclear loci. This provides a possible mechanism for anole speciation on other Caribbean islands.     

Out of Cuba: overwater dispersal and speciation among lizards in the Anolis carolinensis subgroup

Overwater dispersal and subsequent allopatric speciation contribute importantly to the species diversity of West Indian Anolis lizards and many other island radiations. Here we use molecular phylogenetic analyses to assess the contribution of overwater dispersal to diversification of the Anolis carolinensis subgroup, a clade comprising nine canopy-dwelling species distributed across the northern Caribbean. Although this clade includes some of the most successful dispersers and colonists in the anole radiation, the taxonomic status and origin of many endemic populations have been ambiguous. New mitochondrial and nuclear DNA sequences from four species occurring on small islands or island banks (Anolis brunneus, Anolis longiceps, Anolis maynardi, Anolis smaragdinus) and one species from the continental United States (A. carolinensis) are presented and analysed with homologous sequences sampled from related species on Cuba (Anolis allisoni and Anolis porcatus). Our analyses confirm that all five non-Cuban species included in our study represent distinct, independently evolving lineages that warrant continued species recognition. Moreover, our results support Ernest Williams's hypothesis that all of these species originated by overseas colonization from Cuban source populations. However, contrary to Williams's hypothesis of Pleistocene dispersal, most colonization events leading to speciation apparently occurred earlier, in the late Miocene-Pliocene. These patterns suggest that overwater dispersal among geologically distinct islands and island banks is relatively infrequent in anoles and has contributed to allopatric speciation. Finally, our results suggest that large Greater Antillean islands serve as centres of origin for regional species diversity.