Sex Differences In Dispersal Research Articles

Sex ratio of Western Bluebirds Sialia mexicana is mediated by phenology and clutch size.

Mothers may produce more of one sex to maximize their fitness if there are differences in the cost of producing each sex or there are differences in their relative reproductive value. Breeding date and clutch size are known to influence offspring sex ratios in birds through sex differences in dispersal, social behaviours, differential mortality, and available food resources. We tested if breeding date, clutch size and drought conditions influenced offspring sex ratios in a sexually size-monomorphic species, the Western Bluebird, by interrogating a 21-year dataset. After controlling for differential mortality, we found that hatch dates late in the breeding season were associated with the production of more females, suggesting that the value of producing males declines as the breeding season progresses. When clutch size was taken into account, small clutches yielded significantly more females late in the breeding season compared to the early and middle parts of the breeding season that produced significantly more males. Large clutches early in the season tended to produce more females, although this was not significant. Drought severity was not correlated with sex ratio adjustment. We propose and discuss several explanations for these patterns, including male offspring, but not female offspring, acting as helpers, increased female nestling provisioning late in the breeding season, differences in food abundance, and egg-laying order. Future work will help to uncover the mechanisms leading to these patterns. Identifying patterns and mechanisms of sex ratio skew from long-term datasets is important for informing predictions regarding life-history trade-offs in wildlife populations.

Genetic evidence for sex-biased dispersal and cryptic diversity in the greater horseshoe bat, Rhinolophus ferrumequinum

Dispersal plays an important role in the ecological and evolutionary processes of natural populations. Mating behavior (or mating system) is a critical factor shaping dispersal patterns and extents in social mammals, sometimes driving the evolution of sex-biased dispersal. Using molecular markers with contrasting modes of inheritance (mitochondrial DNA and nuclear microsatellites), we determined the population genetic structure and evolutionary history of the great horseshoe bat, Rhinolophus ferrumequinum inhabiting eleven national parks of South Korea, being known as a biodiversity hotspot. Despite apparent matrilineal structure observed over space, there was weak nuclear geographic structure, suggesting female philopatry with male-biased dispersal. The analyses indicated the signal of nonrandom mating (i.e. inbreeding), which is at least partly due to female’s sedentary lifestyle. The large-scale phylogenetic analysis revealed unexpected deep divergence among three distinct clades (Southwest China, East China, and Northeast Asia including South Korea), suggesting these may possibly represent cryptic species complex in R. ferrumequinum. Our findings of sex differences in dispersal in R. ferrumequinum inform conservation managements to enhance the population connectivity among the national parks through promoting female dispersal. Our study also highlights cryptic species diversity in a temperate bat that should have a priority for conservation.

Effect of parental phenotype on dispersal, growth and maturation of offspring in wild masu salmon (Oncorhynchus masou)

Offspring traits are influenced by complex interactions among parent genotypes and phenotypes. However, ecological studies of these effects have tended to focus on one of either maternal or paternal influences. In this study, we investigated the effects of both parental phenotypes on offspring dispersal, growth and early sexual maturity in masu salmon. We used wild-caught parental fish in a half-sib mating design that allowed comparison of offspring from males of two different life-history types (precocious males that had lived only in fresh water and anadromous males that had migrated to the sea). These males were mated with anadromous females and the eggs planted in natural streams in three different years. Natal dispersal distance depended on offspring sex, body size and paternal life history: female offspring moved further downstream than males, whilst daughters of precocious fathers tended to move further downstream than those of anadromous sires. There was a maternal effect on offspring growth, with larger eggs resulting in larger offspring at least until these became precociously mature at the end of the first summer. However, while faster growing male offspring were more likely to become precociously mature, there was no evidence that the probability of precocious maturation was influenced by parental life history. We conclude that, although body size of young salmon was significantly influenced by egg size and there were sex differences in dispersal, their growth rate and divergence in life history types were mainly environmentally driven.

Evolutionary Consequences of Sex-Specific Selection in Variable Environments: Four Simple Models Reveal Diverse Evolutionary Outcomes.

The evolutionary trajectories of species with separate sexes depend on the effects of genetic variation on female and male traits as well as the direction and alignment of selection between the sexes. Classical theory has shown that evolution is equally responsive to selection on females and males, with natural selection increasing the product of the average relative fitness of each sex over time. This simple rule underlies several important predictions regarding the maintenance of genetic variation, the genetic basis of adaptation, and the dynamics of "sexually antagonistic" alleles. Nevertheless, theories of sex-specific selection overwhelmingly focus on evolution in constant environments, and it remains unclear whether they apply under changing conditions. We derived four simple models of sex-specific selection in variable environments and explored how conditions of population subdivision, the timing of dispersal, sex differences in dispersal, and the nature of environmental change mediate the evolutionary dynamics of sex-specific adaptation. We find that these dynamics are acutely sensitive to ecological, demographic, and life-history attributes that vary widely among species, with classical predictions breaking down in contexts of environmental heterogeneity. The evolutionary rules governing sex-specific adaptation may therefore differ between species, suggesting new avenues for research on the evolution of sexual dimorphism.

Sex-biased breeding dispersal is predicted by social environment in birds.

Sex‐biased dispersal is common in vertebrates, although the ecological and evolutionary causes of sex differences in dispersal are debated. Here, we investigate sex differences in both natal and breeding dispersal distances using a large dataset on birds including 86 species from 41 families. Using phylogenetic comparative analyses, we investigate whether sex‐biased natal and breeding dispersal are associated with sexual selection, parental sex roles, adult sex ratio (ASR), or adult mortality. We show that neither the intensity of sexual selection, nor the extent of sex bias in parental care was associated with sex‐biased natal or breeding dispersal. However, breeding dispersal was related to the social environment since male‐biased ASRs were associated with female‐biased breeding dispersal. Male‐biased ASRs were associated with female‐biased breeding dispersal. Sex bias in adult mortality was not consistently related to sex‐biased breeding dispersal. These results may indicate that the rare sex has a stronger tendency to disperse in order to find new mating opportunities. Alternatively, higher mortality of the more dispersive sex could account for biased ASRs, although our results do not give a strong support to this explanation. Whichever is the case, our findings improve our understanding of the causes and consequences of sex‐biased dispersal. Since the direction of causality is not yet known, we call for future studies to identify the causal relationships linking mortality, dispersal, and ASR.

Evolutionary and demographic processes shaping geographic patterns of genetic diversity in a keystone species, the African forest elephant (Loxodonta cyclotis).

The past processes that have shaped geographic patterns of genetic diversity may be difficult to infer from current patterns. However, in species with sex differences in dispersal, differing phylogeographic patterns between mitochondrial (mt) and nuclear (nu) DNA may provide contrasting insights into past events. Forest elephants (Loxodonta cyclotis) were impacted by climate and habitat change during the Pleistocene, which likely shaped phylogeographic patterns in mitochondrial (mt) DNA that have persisted due to limited female dispersal. By contrast, the nuclear (nu) DNA phylogeography of forest elephants in Central Africa has not been determined. We therefore examined the population structure of Central African forest elephants by genotyping 94 individuals from six localities at 21 microsatellite loci. Between forest elephants in western and eastern Congolian forests, there was only modest genetic differentiation, a pattern highly discordant with that of mtDNA. Nuclear genetic patterns are consistent with isolation by distance. Alternatively, male‐mediated gene flow may have reduced the previous regional differentiation in Central Africa suggested by mtDNA patterns, which likely reflect forest fragmentation during the Pleistocene. In species like elephants, male‐mediated gene flow erases the nuclear genetic signatures of past climate and habitat changes, but these continue to persist as patterns in mtDNA because females do not disperse. Conservation implications of these results are discussed.

Estimating adult sex ratios in nature.

Adult sex ratio (ASR, the proportion of males in the adult population) is a central concept in population and evolutionary biology, and is also emerging as a major factor influencing mate choice, pair bonding and parental cooperation in both human and non-human societies. However, estimating ASR is fraught with difficulties stemming from the effects of spatial and temporal variation in the numbers of males and females, and detection/capture probabilities that differ between the sexes. Here, we critically evaluate methods for estimating ASR in wild animal populations, reviewing how recent statistical advances can be applied to handle some of these challenges. We review methods that directly account for detection differences between the sexes using counts of unmarked individuals (observed, trapped or killed) and counts of marked individuals using mark-recapture models. We review a third class of methods that do not directly sample the number of males and females, but instead estimate the sex ratio indirectly using relationships that emerge from demographic measures, such as survival, age structure, reproduction and assumed dynamics. We recommend that detection-based methods be used for estimating ASR in most situations, and point out that studies are needed that compare different ASR estimation methods and control for sex differences in dispersal.This article is part of the themed issue 'Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies'.

Dispersal, Group Formation and Kinship in the Black-Faced Lion Tamarin (Leontopithecus caissara)

We report on (i) new group formation, (ii) sex differences in dispersal and (iii) dispersal distance over 6 years for 3 social groups of the black-faced lion tamarin (Leontopithecus caissara) in the vicinity of Ariri, São Paulo state, Brazil. The groups were: Bina (monitored for 74 months), BM5 (52 months) and Teca (13 months). Each group was censused once a week and monitored for 3 days each month. Mating opportunities were found to be the incentive for young adult black-faced lion tamarins to either disperse or remain in their kin group. Young adults show delayed dispersal that is related to the cooperative breeding system characteristic of the Callitrichidae and to a low population density which hinders the formation of new breeding pairs. Our findings suggest that in L. caissara (i) both sexes disperse, (ii) successful immigration is related to breeding opportunities in an existing group, (iii) female immigration motivates male emigration and the formation of new groups, and (iv) emigrants tend to form new groups close to their natal groups. These patterns of dispersal and formation of new groups are efficient because the species has been able to avoid loss of genetic diversity despite their small population size.

Genetic analyses suggest no immigration of adult females and their offspring into the Sonso community of chimpanzees in the Budongo Forest Reserve, Uganda

Chimpanzees are frequently used to illustrate the relationship between sex differences in dispersal and sex differences in cooperation in primates and other group-living mammals. Male chimpanzees are highly philopatric, typically remaining in their natal communities for their entire lives to cooperate with related males in competition against less related males from other groups, whereas females typically disperse once at adolescence and cooperate with each other less frequently. However, there have been a few reports of dependent male offspring joining groups when their mothers transferred between communities as adults. Although such events are difficult to document, determining how often they actually occur is important for elucidating the links between philopatry, kinship, and cooperation in both chimpanzees and group-living animals more generally. Here we use genetic analyses to investigate a previous report of a large-scale transfer of many females and their offspring into the Sonso community of chimpanzees in the Budongo Forest Reserve, Uganda. Using autosomal microsatellite genotypes, we assigned a Sonso father to ten of the fourteen putative immigrants, and found that the four putative immigrants for whom we could not assign a Sonso father (perhaps due to incomplete sampling of all Sonso candidate fathers) nevertheless had Y-chromosome microsatellite haplotypes that were common in Sonso males but absent in males from four other chimpanzee communities at Budongo. These results suggest that these putative immigrant females and their offspring were probably actually long-term residents of Sonso whose identifications were delayed by their peripheral or unhabituated status. These results are consistent with other genetic and behavioral evidence showing that male between-community gene flow is exceedingly rare in east African chimpanzees.

Sex and stochasticity affect range expansion of experimental invasions

Understanding and predicting range expansion are key objectives in many basic and applied contexts. Among dioecious organisms, there is strong evidence for sex differences in dispersal, which could alter the sex ratio at the expansion's leading edge. However, demographic stochasticity could also affect leading-edge sex ratios, perhaps overwhelming sex-biased dispersal. We used insects in laboratory mesocosms to test the effects of sex-biased dispersal on range expansion, and a simulation model to explore interactive effects of sex-biased dispersal and demographic stochasticity. Sex-biased dispersal created spatial clines in the sex ratio, which influenced offspring production at the front and altered invasion velocity. Increasing female dispersal relative to males accelerated spread, despite the prediction that demographic stochasticity would weaken a signal of sex-biased dispersal. Our results provide the first experimental evidence for an influence of sex-biased dispersal on invasion velocity, highlighting the value of accounting for sex structure in studies of range expansion.

Forest elephant mitochondrial genomes reveal that elephantid diversification in Africa tracked climate transitions

Among elephants, the phylogeographic patterns of mitochondrial (mt) and nuclear markers are often incongruent. One hypothesis attributes this to sex differences in dispersal and in the variance of reproductive success. We tested this hypothesis by examining the coalescent dates of genetic markers within elephantid lineages, predicting that lower dispersal and lower variance in reproductive success among females would have increased mtDNA relative to nuclear coalescent dates. We sequenced the mitochondrial genomes of two forest elephants, aligning them to mitogenomes of African savanna and Asian elephants, and of woolly mammoths, including the most divergent mitogenomes within each lineage. Using fossil calibrations, the divergence between African elephant F and S clade mitochondrial genomes (originating in forest and savanna elephant lineages, respectively) was estimated as 5.5 Ma. We estimated that the (African) ancestor of the mammoth and Asian elephant lineages diverged 6.0 Ma, indicating that four elephantid lineages had differentiated in Africa by the Miocene-Pliocene transition, concurrent with drier climates. The coalescent date for forest elephant mtDNAs was c. 2.4 Ma, suggesting that the decrease in tropical forest cover during the Pleistocene isolated distinct African forest elephant lineages. For all elephantid lineages, the ratio of mtDNA to nuclear coalescent dates was much greater than 0.25. This is consistent with the expectation that sex differences in dispersal and in variance of reproductive success would have increased the effective population size of mtDNA relative to nuclear markers in elephantids, contributing to the persistence of incongruent mtDNA phylogeographic patterns.

A MODEL FOR GENOMIC IMPRINTING IN THE SOCIAL BRAIN: ADULTS

Genomic imprinting refers to genes that are silenced when inherited via sperm or via egg. The silencing of genes conditional upon their parental origin requires an evolutionary explanation. The most widely accepted theory for the evolution of genomic imprinting-the kinship theory-argues that conflict between maternally inherited and paternally inherited genes over phenotypes with asymmetric effects on matrilineal and patrilineal kin results in self-imposed silencing of one of the copies. This theory has been applied to imprinting of genes expressed in the placenta, and infant brain determining the allocation of parental resources being the source of conflict parental promiscuity. However, there is growing evidence that imprinted genes are expressed in the postinfant brain where parental promiscuity per se is no longer a source of conflict. Here, we advance the kinship theory by developing an evolutionary model of genomic imprinting in adults, driven by intragenomic conflict over allocation to parental versus communal care. We consider the role of sex differences in dispersal and variance in reproductive success as sources of conflict. We predict that, in hominids and birds, parental care will be expressed by maternally inherited genes. In nonhominid mammals, we predict more diversity, with some mammals showing the same pattern and other showing the reverse. We use the model to interpret experimental data on imprinted genes in the house mouse: specifically, paternally expressed Peg1 and Peg3 genes, underlying maternal care, and maternally expressed Gnas and paternally expressed Gnasxl genes, underlying communal care. We also use the model to relate ancestral demography to contemporary imprinting disorders of adults, in humans and other taxa.

A MODEL FOR GENOMIC IMPRINTING IN THE SOCIAL BRAIN: JUVENILES

What are imprinted genes doing in the adult brain? Genomic imprinting is when a gene's expression depends upon parent of origin. According to the prevailing view, the "kinship theory" of genomic imprinting, this effect is driven by evolutionary conflicts between genes inherited via sperm versus egg. This theory emphasizes conflicts over the allocation of maternal resources, and focuses upon genes that are expressed in the placenta and infant brain. However, there is growing evidence that imprinted genes are also expressed in the juvenile and adult brain, after cessation of parental care. These genes have recently been suggested to underpin neurological disorders of the social brain such as psychosis and autism. Here we advance the kinship theory by developing an evolutionary model of genomic imprinting for social behavior beyond the nuclear family. We consider the role of demography and mating system, emphasizing the importance of sex differences in dispersal and variance in reproductive success. We predict that, in hominids and birds, altruism will be promoted by paternally inherited genes and egoism will be promoted by maternally inherited genes. In nonhominid mammals we predict more diversity, with some mammals showing the same pattern and other showing the reverse. We discuss the implications for the evolution of psychotic and autistic spectrum disorders in human populations with different social structures.

Sex Differences in Dispersal and the Evolution of Helping and Harming

In this article, we explore the impact of sex-biased dispersal on local relatedness and on selection for helping and harming behavior among males and females. We show that in a patch-structured population, when there is a marked sex bias in dispersal, selection will almost always favor harming behavior among individuals of the sex more prone to dispersal. This result holds regardless of the effects of mating skew or overlapping generations. Selection may well also favor helping behavior among individuals of the philopatric sex, particularly if there is generational overlap, but this is less likely to occur if individuals of the philopatric sex compete more intensely for fewer breeding opportunities. In this last case, if generational overlap is low and mating skew pronounced, the result may be selection for harming behavior among both males and females. In general, the rate of dispersal and the level of relatedness among individuals of one sex do not reliably predict their level of helping or harming behavior; selection on either males or females depends on the dispersal of both sexes.

Sex differences in responsiveness to begging in a cooperative mammal

In species where young are provisioned by both parents, males commonly contribute less to parental care than females, and are less responsive to variation in begging rates. Similar differences in the care of young occur among adults in cooperative breeders, but fewer studies have investigated whether these are associated with differences in responsiveness. Here, we present results from a playback experiment investigating responsiveness to begging in the meerkat (Suricata suricatta), a cooperatively breeding mammal. Although increased begging rate raised the feeding rate of adults of both sexes, there was no consistent tendency for females to be more responsive than males. However, when we examined changes in the proportion of food items found that were fed to pups (generosity), we found that females were more responsive than males to increased begging rate. These results can be explained in terms of sex differences in dispersal: in meerkats, females are philopatric and receive considerable benefits from investing in young, both directly, by increasing group size, and indirectly, by recruiting helpers if they inherit the breeding position. In addition, they emphasize that generosity provides a more sensitive measure of responsiveness to begging than feeding rate, as it accounts for variation in foraging success.

Relationship between age and activity varies by sex in titi monkeys (Callicebus cupreus)

Motor activity increases during development and typically peaks before reproductive maturity. Males may become more active than do females, and this sex difference in activity may be a mechanism contributing to sex-biased dispersal. The generality of the link between sex differences in activity and sex differences in dispersal would be strengthened with evidence of greater female, as compared to male, activity during development in a species with a female bias in dispersal. Titi monkeys are a good model for such an investigation because subadult females leave their natal group at an earlier age than do subadult males. This study examines whether developing female titi monkeys become more active with age than do developing male titi monkeys. Locomotor activity of 13 female and 8 male captive titi monkeys was measured as they matured from initial ambulatory independence (6 months of age) to reproductive maturity (24 months). Increased activity of females was associated most strongly with increasing age. Increased activity of males, however, was associated most strongly with repeated testing. Compared to maturing males, greater activity of maturing females may underlie the earlier dispersal of female titi monkeys that has been reported.

Whip it good! Geographic consistency in male songs and variability in female songs of the duetting eastern whipbird Psophodes olivaceus

Geographic variation in male bird songs has been studied extensively, but there have been few investigations of geographic variation in female songs or sex differences in patterns of geographic variation. We compared patterns of variation in male and female songs of eastern whipbirds Psophodes olivaceus by analyzing recordings from 16 populations across the species’ geographic range in eastern Australia. We found remarkably different patterns of geographic variation between the sexes. Female eastern whipbird songs are easily categorized into discrete song types. Song types are shared between nearby females, but female songs show pronounced differences at a continental scale. In contrast, male eastern whipbird songs show high consistency throughout the species’ geographic range. All recorded males share the ability to transpose the frequency of the introductory whistle and most recorded males share the ability to vary the direction of the slope of the terminal whip crack. For eight of nine measured variables, female songs show significantly higher levels of variation than male songs. We discuss whether sex differences in dispersal, song learning strategies, and song function may explain these sex differences in patterns of song variation. We suggest that eastern whipbirds have experienced a decoupling of male and female song learning strategies and that the songs of each sex have responded to different selective pressures in the context of countersinging interactions. We speculate that consistency in male songs throughout the geographic range of eastern whipbirds may arise through female preference for males that perform large bandwidth whip cracks.

Sex‐biased dispersal in a salmonid fish: implications for growth rate and survival

I tested the hypothesis that dispersal is sex‐biased in an unexploited population of brook trout (Salvelinus fontinalis Mitchill). Based on the assumptions that trout are promiscuous and that reproductive success is limited primarily by either number of mates (males) or fecundity (females), I predicted that males would disperse greater distances than females. I also tested the hypothesis that trout populations comprise stationary and mobile individuals, predicting that males have greater mobility than females. Based on a 5‐year, mark‐recapture study of almost 1000 fish, there was strong support for the hypothesis of male‐biased dispersal. On average, males dispersed 2·5 times as far as females; during the spawning period only, male dispersal exceeded that by females almost four‐fold. Both sexes were heterogeneous with respect to movement, with a lower incidence of mobility among females than males. Sex differences in dispersal may have been responsible for sex biases in seasonal growth. Importantly, growth rate was positively associated with survival, independent of the effects of body size. Sex‐biased dispersal may (1) reduce mate competition among male kin, (2) decrease the probability that males will reproduce with related females, and (3) have important implications for life history.

Dispersal, vaccination and regression of immune defence organs

The thymus in vertebrates and the bursa of Fabricius in birds regress before reproduction, while the immunological information of these organs is maintained as cell memory. Regression at a certain age presupposes that individuals have achieved exposure to a large fraction of parasites in the environment. Here we present a new scenario for regression of immune defence organs, based on optimality reasoning. This scenario links early involution of immune defence organs with (1) effects of exposure to parasites on adaptive immune responses to these parasites, (2) exposure to local parasite communities during natal dispersal and migration as a means of “vaccination” against local parasites, and (3) the function of visits to future breeding sites by juveniles as a means of exposure to local parasites. This scenario provides explanations for why natal dispersal is longer than breeding dispersal, for sex differences in dispersal, and for why the bursa of Fabricius regresses relatively early in life among bird species with delayed start of reproduction.

Dispersal and extra‐territorial prospecting by slender‐tailed meerkats (Suricata suricatta) in the south‐western Kalahari

Dispersal in slender‐tailed meerkats or suricates, Suricata suricatta, in the south‐western Kalahari occurred mainly during the early breeding season, and was age‐ and sex‐dependent. Among yearlings, more males than females were immigrants, but more females than males disappeared. There were no sex differences in dispersal among two‐year‐olds, but among animals aged three years or older, more males than females emigrated. Most dispersers moved into adjacent bands or joined other transients, and females apparently suffered higher rates of mortality than males. Kinship with the same‐sex or opposite‐sex breeder had no discernible effect on the likelihood of dispersing. Both males and females made prospecting forays to other groups, apparently to assess dispersal and breeding opportunities. Males made frequent and repeated forays, often in coalitions with other band members or transients, whereas prospecting by females was generally solitary, and they were not known to make multiple forays. Prospecting males successfully took over dominance of two bands, and attempted to take over bands on three other occasions. Animals attempting to join or follow a band (trailers) behaved submissively and were readily chased by residents, whereas those attempting a dominance takeover (invaders) scent‐marked at a high rate and showed no submissive behaviours. Dispersing meerkats maximized reproductive success by increasing their mating opportunities, while animals which delayed dispersal received indirect benefits by helping to raise kin.