Dispersal and fighting in male pollinating fig wasps

For more than two decades, it has been the dogma that the males of pollinating fig wasps do not fight and that they only mate in their native fig. Their extreme degree of local mating leads to highly female biased sex ratios that should eliminate the benefits of fighting and dispersal by males. Furthermore, males sharing a fig are often brothers, and fighting may be barred by kin selection. Therefore, theory supported the presumed absence of fighting and dispersal in pollinating fig wasp males. However, we report here that in pollinating fig wasps, fighting between brothers evolved at least four and possibly six time, and dispersal by males at least twice. This finding supports the idea that competition between relatives can cancel the ameliorating effects of relatedness. The explanation to this evolutionary puzzle, as well as the consequences of male dispersal and fighting, opens the doors to exciting new research.     

No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.     

Sex‐biased dispersal: a review of the theory

Dispersal is ubiquitous throughout the tree of life: factors selecting for dispersal include kin competition, inbreeding avoidance and spatiotemporal variation in resources or habitat suitability. These factors differ in whether they promote male and female dispersal equally strongly, and often selection on dispersal of one sex depends on how much the other disperses. For example, for inbreeding avoidance it can be sufficient that one sex disperses away from the natal site. Attempts to understand sex‐specific dispersal evolution have created a rich body of theoretical literature, which we review here. We highlight an interesting gap between empirical and theoretical literature. The former associates different patterns of sex‐biased dispersal with mating systems, such as female‐biased dispersal in monogamous birds and male‐biased dispersal in polygynous mammals. The predominant explanation is traceable back to Greenwood's ( 1980 ) ideas of how successful philopatric or dispersing individuals are at gaining mates or the resources required to attract them. Theory, however, has developed surprisingly independently of these ideas: models typically track how immigration and emigration change relatedness patterns and alter competition for limiting resources. The limiting resources are often considered sexually distinct, with breeding sites and fertilizable females limiting reproductive success for females and males, respectively. We show that the link between mating system and sex‐biased dispersal is far from resolved: there are studies showing that mating systems matter, but the oft‐stated association between polygyny and male‐biased dispersal is not a straightforward theoretical expectation. Here, an important understudied factor is the extent to which movement is interpretable as an extension of mate‐searching (e.g. are matings possible en route or do they only happen after settling in new habitat – or can females perhaps move with stored sperm). We also point out other new directions for bridging the gap between empirical and theoretical studies: there is a need to build Greenwood's influential yet verbal explanation into formal models, which also includes the possibility that an individual benefits from mobility as it leads to fitness gains in more than one final breeding location (a possibility not present in models with a very rigid deme structure). The order of life‐cycle events is likewise important, as this impacts whether a departing individual leaves behind important resources for its female or male kin, or perhaps both, in the case of partially overlapping resource use.     

Female‐biased dispersal in a bat with a female‐defence mating strategy

The ultimate causes for predominant male‐biased dispersal (MBD) in mammals and female‐biased dispersal (FBD) in birds are still subject to much debate. Studying exceptions to general patterns of dispersal, for example, FBD in mammals, provides a valuable opportunity to test the validity of proposed evolutionary pressures. We used long‐term behavioural and genetic data on individually banded Proboscis bats (Rhynchonycteris naso) to show that this species is one of the rare mammalian exceptions with FBD. Our results suggest that all females disperse from their natal colonies prior to first reproduction and that a substantial proportion of males are philopatric and reproduce in their natal colonies, although male immigration has also been detected. The age of females at first conception falls below the tenure of males, suggesting that females disperse to avoid father–daughter inbreeding. Male philopatry in this species is intriguing because Proboscis bats do not share the usual mammalian correlates (i.e. resource‐defence polygyny and/or kin cooperation) of male philopatry. They have a mating strategy based on female defence, where local mate competition between male kin is supposedly severe and should prevent the evolution of male philopatry. However, in contrast to immigrant males, philopatric males may profit from acquaintance with the natal foraging grounds and may be able to attain dominance easier and/or earlier in life. Our results on Proboscis bats lent additional support to the importance of inbreeding avoidance in shaping sex‐biased dispersal patterns and suggest that resource defence by males or kin cooperation cannot fully explain the evolution of male philopatry in mammals.     

Behavioural inbreeding avoidance in wild African elephants

The costs of inbreeding depression, as well as the opportunity costs of inbreeding avoidance, determine whether and which mechanisms of inbreeding avoidance evolve. In African elephants, sex-biased dispersal does not lead to the complete separation of male and female relatives, and so individuals may experience selection to recognize kin and avoid inbreeding. However, because estrous females are rare and male-male competition for mates is intense, the opportunity costs of inbreeding avoidance may be high, particularly for males. Here we combine 28 years of behavioural and demographic data on wild elephants with genotypes from 545 adult females, adult males, and calves in Amboseli National Park, Kenya, to test the hypothesis that elephants engage in sexual behaviour and reproduction with relatives less often than expected by chance. We found support for this hypothesis: males engaged in proportionally fewer sexual behaviours and sired proportionally fewer offspring with females that were natal family members or close genetic relatives (both maternal and paternal) than they did with nonkin. We discuss the relevance of these results for understanding the evolution of inbreeding avoidance and for elephant conservation.     

Inbreeding avoidance mechanisms: dispersal dynamics in cooperatively breeding southern pied babblers

1.?Breeding with kin can reduce individual fitness through the deleterious effects of inbreeding depression. Inbreeding avoidance mechanisms are expected to have developed in most species, and especially in cooperatively breeding species where individuals may delay dispersal until long after sexual maturity. Such potential mechanisms include sex-biased dispersal and avoidance of kin known through associative learning. 2.?The investigation of inbreeding avoidance through dispersal dynamics can be enhanced by combining fine-scale population genetic structure data with detailed behavioural observations of wild populations. 3.?We investigate possible inbreeding avoidance in a wild population of cooperatively breeding southern pied babblers (Turdoides bicolor). A combination of genetic, geographic and observational data is used to examine fine-scale genetic structure, dispersal (including sex-biased dispersal) and inheritance of dominance in cooperatively breeding groups. 4.?Unusually, sex-bias in dispersal distance does not occur. Rather, individuals appear to avoid inbreeding through two routes. First, through dispersal itself: although both males and females disperse locally, they move outside the range within which genetically similar individuals are usually found, going twice as far from natal groups as from non-natal groups. Second, through avoidance of familiar group members as mates: individuals inherit a dominant position in the natal group only when an unrelated breeding partner is present. 5.?This study uses spatial genetic analyses to investigate inbreeding avoidance mechanisms in a cooperative breeder and shows that individuals of both sexes can avoid inbreeding through a dispersal distance mechanism. While it appears that dispersal allows most individuals to move beyond the range of closely related kin, matings may still occur between distant kin. Nevertheless, any costs of breeding with a distant relative may be outweighed by the benefits of local dispersal and the immense fitness gains available from attaining a breeding position.     

Sex-biased dispersal in eastern chipmunks, Tamias striatus

I investigated the effect of male mate competition and inbreeding avoidance on natal dispersal of chipmunks by longitudinally monitoring known individuals from 1986 to 1990. Natal males exhibited greater absolute and effective dispersal distances but dispersed at the same proportion as natal females. Recruitment of juvenile males was negatively affected by density of resident males, but there was no evidence of local mate competition among male kin. Analysis of the spatial distribution of neighbors showed that natal males settled farther from their mothers than did their female siblings and farther than unrelated juvenile males. In addition, mothers apparently tolerated daughters as close neighbors and occasionally shared den sites with grandprogeny. Sexually mature males were never neighbors of their mothers and were never observed at maternal mating bouts. Males may disperse to improve reproductive opportunities by avoiding competition with resident males, and by increasing access to unrelated females. Maternal tolerance of daughters but not sons may result in the close affiliation between mothers and daughters, and indirectly contribute to dispersal of natal males. Hence male-biased dispersal could be a consequence of mate competition and maternal avoidance of incestuous matings. This revised version was published online in July 2006 with corrections to the Cover Date.     

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.     

PROBLEMS WITH TESTING INBREEDING AVOIDANCE: THE CASE OF THE COLLARED FLYCATCHER

Four year's data on collared flycatchers, Ficedula albicollis, breeding in a nestbox plot on the island of Gotland, Sweden, was used to investigate whether individuals avoid mating with close kin (i.e., parents or sibs). Only one case of close inbreeding (0.5% of all pairs) was observed during the years of study. The observed frequency of close inbreeding was compared to expected frequencies based on two different null models. Assuming no inbreeding avoidance behaviors (e.g., dispersal or kin recognition), but taking into account the fact that mortality, and different arrival and pairing times of individuals reduce the probability of mating with close kin, the expected frequency of close inbreeding is 10% and 15% for female and male recruits (i.e., born in the study plot), respectively. However, assuming mating to be random within the study plot reduced the expected frequency of close inbreeding to 1% or less for both males and females. Consequently, conclusions drawn concerning inbreeding avoidance depend on the null model used. Contrasting estimated costs of tolerating close inbreeding with those of avoiding it (by dispersal to other plots), however, suggests that the costs of avoiding close inbreeding are substantially greater than those of tolerating it. Therefore, although inbreeding avoidance cannot be rejected as a cause of dispersal of this species, it is not the primary cause, and particularly not for sex-biased dispersal. The general problems of investigating inbreeding avoidance are discussed. It is argued that all previous null models based on random mating in finite populations produce expected frequencies of close inbreeding that in fact include inbreeding avoidance, since they implicitly assume random dispersal within a finite population. Thus, comparisons between observed and expected frequencies of close inbreeding based on random mating are inadequate. The most promising method of investigating inbreeding avoidance is to experimentally study individual movements and mating preferences in the presence and absence of close kin.     

A comparative approach to testing hypotheses for the evolution of sex‐biased dispersal in bean beetles

Understanding the selective forces that shape dispersal strategies is a fundamental goal of evolutionary ecology and is increasingly important in changing, human‐altered environments. Sex‐biased dispersal (SBD) is common in dioecious taxa, and understanding variation in the direction and magnitude of SBD across taxa has been a persistent challenge. We took a comparative, laboratory‐based approach using 16 groups (species or strains) of bean beetles (genera Acanthoscelides, Callosobruchus, and Zabrotes, including 10 strains of one species) to test two predictions that emerge from dominant hypotheses for the evolution of SBD: (1) groups that suffer greater costs of inbreeding should exhibit greater SBD in favor of either sex (inbreeding avoidance hypothesis) and (2) groups with stronger local mate competition should exhibit greater male bias in dispersal (kin competition avoidance hypothesis). We used laboratory experiments to quantify SBD in crawling dispersal, the fitness effects of inbreeding, and the degree of polygyny (number of female mates per male), a proxy for local mate competition. While we found that both polygyny and male‐biased dispersal were common across bean beetle groups, consistent with the kin competition avoidance hypothesis, quantitative relationships between trait values did not support the predictions. Across groups, there was no significant association between SBD and effects of inbreeding nor SBD and degree of polygyny, using either raw values or phylogenetically independent contrasts. We discuss possible limitations of our experimental approach for detecting the predicted relationships, as well as reasons why single‐factor hypotheses may be too simplistic to explain the evolution of SBD.     

Sex biases in kin shoaling and dispersal in a cichlid fish

Animal dispersal is associated with diverse costs and benefits that vary among individuals based on phenotype and ecological conditions. For example, females may disperse when males benefit more from defending territories in familiar environments. Similarly, size differences in dispersal propensity may occur when dispersal costs are size-dependent. When individuals do disperse, they may adopt behavioral strategies that minimize dispersal costs. Dispersing fish, for example, may travel within shoals to reduce predation risks. Further, kin shoaling may augment inclusive fitness by reducing predation of relatives. However, studies are lacking on the role of kin shoaling in dispersal. We explored how sex and size influence dispersal and kin shoaling in the cichlid Neolamprologus caudopunctatus. We microsatellite genotyped over 900 individuals from two populations separated by a potential dispersal barrier, and documented patterns of population structure, migration and within-shoal relatedness. Genetic differentiation across the barrier was greater for smaller than larger fish, suggesting larger fish had dispersed longer distances. Females exhibited weaker genetic differentiation and 11 times higher migration rates than males, indicating longer-distance female-biased dispersal. Small females frequently shoaled with siblings, possibly offsetting dispersal costs associated with higher predation risks. In contrast, small males appeared to avoid kin shoaling, possibly to avoid local resource competition. In summary, long-distance dispersal in N. caudopunctatus appears to be female-biased, and kin-based shoaling by small females may represent a behavioral adaptation that reduces dispersal costs. Our study appears to be the first to provide evidence that sex differences in dispersal influence sex differences in kin shoaling.     

Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric

In cooperative breeders, the tension between the opposing forces of kin selection and kin competition is at its most severe. Although philopatry facilitates kin selection, it also increases the risk of inbreeding. When dispersal is limited, extra-pair paternity might be an important mechanism to avoid inbreeding, but evidence for this is equivocal. The red-winged fairy-wren is part of a genus of cooperative breeders with extreme levels of promiscuity and male philopatry, but is unique in that females are also strongly philopatric. Here, we test the hypothesis that promiscuity is an important inbreeding avoidance mechanism when both sexes are philopatric. Levels of extra-pair paternity were substantial (70% of broods), but did not arise through females mating with their helpers, but via extra-group mating. Offspring were more likely to be sired by extra-pair males when the social pair was closely related, and these extra-pair males were genetically less similar to the female than the social male and thus, inbreeding is avoided through extra-pair mating. Females were consistent in their choice of the extra-pair sire over time and preferred early moulting males. Despite neighbouring males often being close kin, they sired 37% of extra-pair offspring. However, females that gained paternity from neighbours were typically less related to them than females that gained paternity further away. Our study is the first to suggest that mating with both closely related social partners and neighbours is avoided. Such sophistication in inbreeding avoidance strategies is remarkable, as the extreme levels of promiscuity imply that social context may provide little cue to relatedness.     

Natal Dispersal and Philopatry in the Carnivorous Marsupial Phascogale tapoatafa (Dasyuridae)

The proximate and ultimate causes of dispersal in semelparous carnivorous marsupials (Phascogalinae) have previously been hypothesized to be maternal aggression and inbreeding avoidance, respectively. This study tests these hypotheses by exposing 26 litters of Phascogale tapoatafa to a diverse range of social and environmental conditions that potentially affect dispersal (e.g. supplemental feeding, post-weaning desertion by the mother, orphaning, and release of subadults into unoccupied habitat). The mean dispersal age was 162 ± 5.6 d, which is about 3 wk after weaning is complete. Juvenile dispersal was strongly male biased under all conditions, suggesting that extrinsic proximate causes do not adequately account for male emigration. Home range establishment by males was contingent on the presence of females. Half of the monitored daughters were philopatric, and others typically settled adjacent to the natal site, thus possibly enhancing their reproductive potential by occupying an area of known resource quality. Because philopatry increases the risk of incest, females may be selected to preferentially mate with unrelated males (immigrants), when they are available, to avoid inbreeding. If so, the presence of immigrant males would reduce the probability of locally born, related males reproducing at their natal site. Thus inbreeding avoidance by females may create local mate competition among males and select for male dispersal. Emigration also ensured that males avoided inbreeding, but, if they dispersed into unoccupied habitat, male P. tapoatafa often returned to the natal area. This 'boomerang strategy' of returning to mate with related females suggests that, in the absence of conspecifics along the dispersal path of a male, mate competition will be weak at the natal site and female mate choice will not preclude related males. Thus while inbreeding avoidance by either or both sexes is perhaps the most parsimonious explanation of male-biased emigration, dispersal patterns were apparently strongly influenced by additional factors, so that the ultimate causation of the dispersal regime may be more complex.     

Density and genetic relatedness increase dispersal distance in a subsocial organism

Although dispersal distance plays a major role in determining whether organisms will reach new habitats, empirical data on the environmental factors that affect dispersal distance are lacking. Population density and kin competition are two factors theorised to increase dispersal distance. Using the two‐spotted spider mite as a model species, we altered these two environmental conditions and measured the mean dispersal distance of individuals, as well as other attributes of the dispersal kernel. We find that both density and relatedness in the release patch increase dispersal distance. Relatedness, but not density, changes the shape of the dispersal kernel towards a more skewed and leptokurtic shape including a longer ‘fat‐tail’. This is the first experimental demonstration that kin competition can shape the whole distribution of dispersal distances in a population, and thus affect the geographical spread of dispersal phenotypes.     

Intraspecific interactions in the annual legume Medicago minima are shaped by both genetic variation for competitive ability and reduced competition among kin

Documenting if plants exhibit kin competition avoidance in intraspecific plant interactions is relevant both to improve crop growth, and to understand diversity and composition in natural plant communities. However, a number of confounding mechanisms complicates detecting kin competition avoidance from experiments comparing plants growing with kin and non-kin neighbors. We conducted complementary greenhouse experiments using genotypes from four populations of the annual Medicago minima, which in a previous study showed higher survival when interacting with kin relative to non-kin. We show that genotypes vary in kin competition avoidance, and in competitive ability, but find no indication of complementary resource use. Importantly, from our first experiment of root growth behavior, we know that some genotypes exhibit kin competition avoidance. Yet, the variation in competitive ability we find in our second experiment, where plants grow in mini communities together with either kin or unrelated genotypes, can alone explain the variation we observe in growth and biomass among communities. In our case, the genotypes with highest competitive ability were also those that showed kin competition avoidance. This confounding effect obscured the disentangling of mechanisms underlying difference in growth between kin and non-kin interactions. When silencing root exudates by adding activated carbon to a subset of our genotype combinations, we found increased size asymmetry of plants grown together, and mostly in kin communities. This suggests that plants recognize the identity of neighbors via root exudates, and compete less with neighbors recognized as kin. To detect kin competition avoidance we suggest designing experiments that pair unrelated genotypes with similar competitive abilities. Such design, combined with silencing root exudates would be powerful to detect whether plants show kin competition avoidance or not.     

Affinity towards maternal odour and offspring dispersal in the common lizard

Kin competition is known to strongly influence the spacing behaviour of juveniles in the common lizard, a species which is only weakly social and has no parental care. We examined whether variation in offspring dispersal propensity was associated with variation in their ability to discriminate odours of their mothers versus unknown females. We caught pregnant females in two populations and reared them in the laboratory until parturition. Just after birth, we recorded the juvenile response to the odour of either their mother or an unrelated female. Mothers and offspring were then released at the mother's last capture point, and juvenile movement was monitored by recapture for 2 years. Philopatric individuals were more attracted to the odour of their mother and more repulsed by the odour of an unrelated female than dispersers. In this species, ability to discriminate maternal cues appears to be implied in the spacing behaviour of juveniles. Since juvenile males and females reacted in the same way, the main role of mother discrimination is likely to be the avoidance of kin competition by promoting juvenile dispersal. This does not necessary require mother discrimination to imply mother recognition, or not to be implied in other functions such as inbreeding avoidance. Further research is needed to clarify these points. We suggest that context-dependent kin discrimination may be involved in the spacing behaviour of a large number of species, even for those species where other social functions for kin discrimination have been proposed.     

Estimating sex-specific dispersal rates with autosomal markers in hierarchically structured populations

Abstract –A recent study suggests that sex-specific dispersal rates can be quantitatively estimated on the basis of sex- and state-specific (pre- vs. postdispersal) F -statistics. In the present paper, we extend this approach to account for the hierarchical structure of natural populations, and we validate it through individual-based simulations. The model is applied to an empirical data set consisting of 536 individuals (males, females, and predispersal juveniles) of greater white-toothed shrews ( Crocidura russula ), sampled according to a hierarchical design and typed for seven autosomal microsatellite loci. From this dataset, dispersal is significantly female biased at the local scale (breeding-group level), but not at the larger scale (among local populations). We argue that selective pressures on dispersal are likely to depend on the spatial scale considered, and that short-distance dispersal should mainly respond to kin interactions (inbreeding or kin competition avoidance), which exert differential pressure on males and females.     

The evolution of trans-generational altruism: kin selection meets niche construction

A cornerstone result of sociobiology states that limited dispersal can induce kin competition to offset the kin selected benefits of altruism. Several mechanisms have been proposed to circumvent this dilemma but all assume that actors and recipients of altruism interact during the same time period. Here, this assumption is relaxed and a model is developed where individuals express an altruistic act, which results in posthumously helping relatives living in the future. The analysis of this model suggests that kin selected benefits can then feedback on the evolution of the trait in a way that promotes altruistic helping at high rates under limited dispersal. The decoupling of kin competition and kin selected benefits results from the fact that by helping relatives living in the future, an actor is helping individuals that are not in direct competition with itself. A direct consequence is that behaviours which actors gain by reducing the common good of present and future generations can be opposed by kin selection. The present model integrates niche-constructing traits with kin selection theory and delineates demographic and ecological conditions under which altruism can be selected for; and conditions where the 'tragedy of the commons' can be reduced.     

Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla)

We explored two hypotheses related to potential differences between sexes in dispersal behaviour in western lowland gorillas (Gorilla gorilla gorilla). Direct observations suggest that immature females have more opportunities to move between breeding groups than immature males. The distribution of kin dyadic relationships within and between groups does not, however, support this hypothesis. At larger geographical scales, dispersal is likely to be easier for males than females because of the solitary phase most blackbacks experience before founding their own breeding group. However, previous work indicates that males settle preferentially close to male kin. By specifically tracing female and male lineages with mitochondrial and Y-chromosomal genetic markers, we found that male gorillas in the 6000 km2 area we surveyed form a single population whereas females are restricted to the individual sites we sampled and do not freely move around this area. These differences are more correctly described as differences in dispersal distances, rather than differences in dispersal rates between sexes (both sexes emigrate from their natal group in this species). Differences in resource competition and dispersal costs between female and male gorillas are compatible with the observed pattern, but more work is needed to understand if these ultimate causes are responsible for sex-biased dispersal distances in western lowland gorillas.