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.     

Intersexual competition as an explanation for sex-ratio and dispersal biases in polygynous species

In polygynous mammals, it is commonly observed that both sex ratios at birth and dispersal are male biased. This has been interpreted as resulting from low female dispersal causing high female local resource competition, which would select for male-biased sex ratios. However, a female-biased sex ratio can be selected despite lower female than male-biased dispersal. This will occur if the low female dispersal is close to the optimal dispersal rate, while the male dispersal is not close to the optimal dispersal rate. The actual outcome depends on the joint evolution of sex-biased dispersal and sex ratio. Earlier analyses of joint evolution imply that there will be no sex-ratio nor dispersal biases at the joint evolutionarily stable strategy, thus they do not explain the data. However, these earlier analyses assume no intersexual competition for resources. Here, we show that when males and females compete with each other for access to resources, male-biased dispersal will be associated with male-biased birth sex ratio, as is commonly observed. A trend toward male-biased birth sex ratios is also expected if there is intersexual local resource competition and if birth sex ratio is constrained so that it cannot depart from balanced sex ratio.     

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.     

Is offspring dispersal related to male mating status? An experiment with the facultatively polygynous spotless starling

Patterns of natal dispersal are generally sex‐biased in vertebrates, i.e. female‐biased in birds and male‐biased in mammals. Interphyletic comparisons in mammals suggest that male‐biased dispersal occurs in polygynous and promiscuous species where local mate competition among males exceeds local resource competition among females. However, few studies have analysed sex‐biased patterns of dispersal at the individual level, and facultatively polygynous species might offer this opportunity. In the spotless starling, polygynous males exhibit their mating status during courtship carrying higher amounts of green plants to nests than monogamous males. We experimentally incorporated green plants to nests during four years to analyse long‐term consequences on breeding success and offspring recruitment rates. We unexpectedly found that experimental sons recruited farther than experimental daughters, while control daughters recruited farther than control sons. A similar pattern was found using observational information from eight years. We discuss this result in the context of local competition hypothesis and speculate that sons dispersed farther from nests controlled by polygynous males to avoid competition with relatives. The amount of green plants in nests affects female perception of male attractiveness and degree of polygyny, although little is known about proximate mechanisms linking this process with the offspring dispersal behaviour. Our results support the idea that male‐biased dispersal is related to polygyny in a facultatively polygynous bird.     

Female-biased dispersal under conditions of low male mating competition in a polygynous mammal

Sex-biased dispersal is a common phenomenon in birds and mammals. Competition for mates has been argued to be an important selective pressure favouring dispersal. Sexual differences in the level of intrasexual competition may produce asymmetries in the costs-benefits balance of dispersal and philopatry for males and females, which may favour male-biased dispersal in polygynous species such as most mammals. This being the case, condition-dependent dispersal predicts that male-bias should decrease if mating competition relaxes. We test this expectation for red deer, where male-biased dispersal is the norm. In southwestern Spain, red deer populations located in nonfenced hunting estates presented altered structures with sex ratio strongly biased to females and high proportion of young males. As a consequence, mate competition in these populations was lower than in other, most typical red deer populations. We found that, under such conditions of altered population structure, dispersal was female-biased rather than male-biased. Additionally, mate competition positively related to male dispersal but negatively to female dispersal. Other factors such as resource competition, age of individuals and sex ratio were not related to male or female dispersal. Males may not disperse if intrasexual competition is low and then females may disperse as a response to male philopatry. We propose hypotheses related to female mate choice to explain female dispersal under male philopatry. The shift of the sex-biased dispersal pattern along the gradient of mate competition highlights its condition-dependence as well as the interaction between male and female dispersal in the evolution of sex-biased dispersal.     

Male-biased reproduction and sex-ratio adjustment in muskrats

Summary Sex ratios of a population and of litters were sampled in muskrats in Ontario, Canada. Sex ratios of litters sampled from nests were male biased (54% male). Until weaning, no differential costs of producing and rearing male and female young were identified that could account for this greater production of males. Following weaning, however, male-biased dispersal of juveniles from their natal site and more frequent acquisition by females of these sites as breeding sites the following year suggested a greater investment by adult females in female young. Therefore, competition between female siblings for the acquisition of their natal site may be sufficient to result in the greater production of males. In addition, the simultaneous occupation of, and competition between, siblings and parents for the resources of the natal home range may not be necessary for local resource competition to result in a greater production of the dispersing sex. Greater-than-expected binomial variance in sex ratios of litters suggested that adjustment of sex-ratios occurred. However, we were unable to associate the adjustment of litter sex ratios with changes in maternal condition. The greater production of males and the predominance of monogamous associations between adults in this population may have lead to slightly greater variation in male fitness than female fitness. Therefore, a female in better-than-average condition may have benefited by producing more males. Similarly, a lower cost of producing dispersing males may allow nutritionally-stressed females to reduce their total expenditure on offspring by producing more males. Because these experiments were non-manipulative, maternal condition may not have varied sufficiently during this study to detect adjustments of litter sex ratios resulting from either of the above mechanisms acting separately, but the combined effects of small differences in matermal condition and selective pressures operating in the same direction may have resulted in the observed deviation from the binomial.     

Genetic evidence for male-biased dispersal in the three-spined stickleback (Gasterosteus aculeatus)

Sex-biased dispersal is capable of generating population structure in nonisolated populations and may affect adaptation processes when selective conditions differ among populations. Intrasexual competition for local resources and/or mating opportunities predicts a male-biased dispersal in polygynous species and a female bias in monogamous species. The patterns of sex-biased dispersal in birds and mammals are well explained by their respective mating systems, but the picture emerging from fish studies is still mixed. Using neutral genetic markers, we investigated whether there is any evidence for sex-biased dispersal among Baltic Sea populations of the three-spined stickleback ( Gasterosteus aculeatus ). The null hypothesis of non sex-biased dispersal was rejected in favour of male-biased dispersal in this species. As the three-spined stickleback has a polygynous mating system, the observed male bias in dispersal is consistent with the hypothesis that local mate competition might drive the observed pattern. Although more research both on the proximate and ultimate causes behind the observed pattern is needed, our results serve as a first step towards understanding patterns of sex-biased dispersal in this species.     

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.     

The new kid on the block: immigrant males win big whereas females pay fitness cost after dispersal

Dispersal is nearly universal; yet, which sex tends to disperse more and their success thereafter depends on the fitness consequences of dispersal. We asked if lifetime fitness differed between residents and immigrants (successful between‐population dispersers) and their offspring using 29 years of monitoring from North American red squirrels (Tamiasciurus hudsonicus) in Canada. Compared to residents, immigrant females had 23% lower lifetime breeding success (LBS), while immigrant males had 29% higher LBS. Male immigration and female residency were favoured. Offspring born to immigrants had 15–43% lower LBS than offspring born to residents. We conclude that immigration benefitted males, but not females, which appeared to be making the best of a bad lot. Our results are in line with male‐biased dispersal being driven by local mate competition and local resource enhancement, while the intergenerational cost to immigration is a new complication in explaining the drivers of sex‐biased dispersal.     

The mating system of the White-throated Magpie-jay Calocitta formosa and Greenwood's hypothesis for sex-biased dispersal

Greenwood explained the different sex bias in dispersal of birds (usually female biased) and mammals (usually male biased) by a difference in mating systems: male birds primarily defend resources while male mammals primarily defend females. The White-throated Magpie-jay Calocitta formosa is unusual among birds in that females are philopatric and jointly defend permanent resource territories while males disperse before they are 2 years of age. One female in a group is the primary breeder. One male joins the group permanently as her mate. Males that do not have a permanent breeding position circulate among groups and attempt to mate with both the primary breeding female and other group females. Other females feed the primary breeder and her offspring and also pursue other reproductive behaviour, including secondary nesting in the territory and egg dumping into the primary breeder's nest. I argue that the unusual dispersal pattern in this species is a result of the alternative reproductive strategies that can be pursued by males and females excluded from being primary breeders. The White-throated Magpie-jay conforms to Greenwood's predictions: males pursue a mate defence rather than resource defence mating system and they are the dispersing sex. The primary factor influencing alternative reproductive tactics may be asynchronous reproduction among groups during the long breeding season arising from frequent renesting in an area of high nest predation.     

Sex-biased dispersal in a salmonid fish

We tested the hypothesis that dispersal is sex biased in an unexploited population of brook trout, Salvelinus fontinalis, on Cape Race, Newfoundland, Canada. Based on the assumptions that trout are promiscuous and that reproductive success is limited primarily by either number of mates (males) or fecundity (females), we predicted that males would disperse greater distances than females. We also tested the hypothesis that trout populations comprise stationary and mobile individuals, predicting that males have greater mobility than females. Based on a mark-recapture study of 943 individually tagged fishes, 191 of which were recaptured over 5 years, we find strong support for our hypothesis of male-biased dispersal in brook trout. Averaged among all 11 resampling periods, males dispersed 2.5 times as far as females; during the spawning period only, male dispersal exceeded that by females almost fourfold. Both sexes were heterogeneous with respect to movement, with a lower incidence of mobility among females (29.6%) than males (41.1%); mobile males dispersed six times further than mobile females. We conclude that this sex bias reduces mate competition among male kin and decreases the probability that males will reproduce with related females.     

Males' evolutionary responses to experimental removal of sexual selection

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.     

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.     

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.     

Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina

Understanding why females mate multiply is a major issue in evolutionary ecology. We investigated the consequences of an asynchronous arrival pattern on male competition and multiple paternity in the apparently monoandrous agile frog ( Rana dalmatina ). The largest frogs arrived first and both males and females lost weight significantly during the spawning period. Asynchronous arrival at breeding sites resulted in a male-biased operational sex ratio (OSR). The OSR was more strongly male-biased at the beginning and at the end of the breeding period when the number of satellite males increased. All females mated only once, but multiple paternity within clutches occurred at the beginning and the end of the breeding period. The influence of asynchronous arrival and biased sex ratio suggests that reduced variance or bet-hedging promoting female fitness had only a reduced role in the evolution of polyandry, and polyandry is likely to be associated with male benefits. Polyandry in frogs can be explained either by forced mating as a result of sexual conflict or by clutch piracy. By modifying intrasexual competition, asynchronous arrival and changes in OSR may have a decisive influence upon the evolution of mating systems and favour both polyandry and stable coexistence of alternative mating behaviour.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 191–200.     

Why do female migratory birds arrive later than males?

1. In migratory birds males tend to arrive first on breeding grounds, except in sex-role reversed species. The two most common explanations are the rank advantage hypothesis, in which male-male competition for breeding sites drives stronger selection for early arrival in males than females, and the mate opportunity hypothesis, which relies on sexual selection, as early arrival improves prospects of mate acquisition more for males than for females. 2. To date, theoretical work has focused on selection for early arrival within a single sex, usually male. However, if fitness depends on territory quality, selection for early arrival should operate on both sexes. Here we use two independent modelling approaches to explore the evolution of protandry (male-first arrival) and protogyny (female-first arrival) under the rank advantage and mate opportunity hypotheses. 3. The rank advantage hypothesis, when operating alone, fails to produce consistent patterns of protandry, despite our assumption that males must occupy territories before females. This is because an individual of either sex benefits if it out-competes same-sex competitors. Rather than promoting protandry, the rank advantage mechanism can sometimes result in protogyny. Female-female competition is stronger than male-male competition early in the season, if females compete for a resource (territories occupied by males) that is initially less common than the resource of interest to males (unoccupied territories). 4. Our results support the mate opportunity hypothesis as an explanation of why protandry is the norm in migratory systems. Male-biased adult sex ratios and high levels of sperm competition (modelled as extra-pair young: EPY) both produce protandry as a result of sexual selection. Protogyny is only observed in our models with female-biased sex ratios and low EPY production. 5. We also show that the effects of sex ratio biases are much stronger than those of EPY production, explore the evidence for sex ratio biases and extra-pair paternity in migratory species and suggest future research directions.     

Female-biased natal dispersal in the Siberian flying squirrel

Natal dispersal is usually sex biased in birds and mammals.Female-biased natal dispersal is the prevailing pattern in birdsbut is rare among mammals. Hypotheses explaining sex bias indispersal include the mate-defense mating hypothesis, whichpredicts male-biased dispersal, the resource-defense hypothesispredicting female-biased dispersal, and the competition hypothesis,which predicts that if dispersal is caused by competition forresources between sexes, then the subdominant sex will disperse.We studied natal dispersal of Siberian flying squirrels Pteromysvolans using radio telemetry in Southern Finland in 1996–2004.Of 86 juveniles that survived over the dispersal period, almostall young females dispersed from the natal site, whereas almost40% of males were philopatric. Dispersal was farther for femalesthan males. Females began dispersal on average 2 weeks earlierthan males and were lighter in mass at the onset of dispersalthan later dispersing males. No mate- or resource-defense matingsystem could be found among males, but females seemed to defendnest and apparently food resources, in contrast to the expectationof dispersal bias in resource-defense systems. Competition forresources between sexes does not explain female bias either:in the flying squirrel, the female seems to be the dominantsex. We propose that young females are subordinate to theirmothers and have to disperse to find a vacant, suitable sitefor reproduction.     

Birth sex ratio in captive mammals: Patterns,biases, and the implications for management and conservation

Sex allocation theory predicts that a female should produce the offspring of the sex that most increases her own fitness. For polygynous species, this means that females in superior condition should bias offspring production toward the sex with greater variation in lifetime reproductive success, which is typically males. Captive mammal populations are generally kept in good nutritional condition with low levels of stress, and thus populations of polygynous species might be expected to have birth sex ratios biased toward males. Sex allocation theory also predicts that when competition reduces reproductive success of the mother, she should bias offspring toward whichever sex disperses. These predicted biases would have a large impact on captive breeding programs because unbalanced sex ratios may compromise use of limited space in zoos. We examined 66 species of mammals from three taxonomic orders (primates, ungulates, and carnivores) maintained in North American zoos for evidence of birth sex ratio bias. Contrary to our expectations, we found no evidence of bias toward male births in polygynous populations. We did find evidence that birth sex ratios of primates are male biased and that, within primates, offspring sex was biased toward the naturally dispersing sex. We also found that most species experienced long contiguous periods of at least 7 years with either male‐ or female‐biased sex ratios, owing in part to patterns of dispersal (for primates) and/or to stochastic causes. Population managers must be ready to compensate for significant biases in birth sex ratio based on dispersal and stochasticity. Zoo Biol 19:11–25, 2000. © 2000 Wiley‐Liss, Inc.     

Evolutionary significance of promiscuity in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae)

The short- and long-term consequences of monogamy and promiscuity in an aphidophagous ladybird, Propylea dissecta (Mulsant) in terms of reproductive performance and offspring fitness were investigated. Promiscuous females were more fecund and laid more viable eggs than monogamous ones. Amongst promiscuous females, those mated with multiple males (freedom for mate choice) had significantly higher reproductive output than those mated daily with a new unmated male. The increased reproductive output of females mated with an unmated male each day in comparison to monogamous ones might possibly be a result of their increased ejaculate size. The further increase in reproductive output, when a female was allowed to choose a mate, may be because of repeated preferential mating with the fitter males. Results on long-term consequences of promiscuity revealed faster development and increased survival in offspring of promiscuous females at 25, 27 and 30 degrees C. The percent adult emergence was more strongly influenced than development by the mating regime. There were no statistically significant differences in survival of offspring of promiscuous females (mate choice) at the three temperatures, while the percent survival of offspring of monogamous females differed significantly. Offspring of promiscuous females (mate choice) were fittest in terms of development and survival, which indicates their probable better genetic constitution and subsequently that of chosen mates. Thus, promiscuity has both short- and long-term benefits and is advantageous to ladybirds. The presence of long-term benefits in terms of fitter offspring probably indicates the evolutionary rationale behind the prevalence of promiscuity in ladybirds.     

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.