Neither genetic nor observational data alone are sufficient for understanding sex-biased dispersal in a social-group-living species

Complex sex-biased dispersal patterns often characterize social-group-living species and may ultimately drive patterns of cooperation and competition within and among groups. This study investigates whether observational data or genetic data alone can elucidate the potentially complex dispersal patterns of social-group-living black and white colobus monkeys ( Colobus guereza , 'guerezas'), or whether combining both data types provides novel insights. We employed long-term observation of eight neighbouring guereza groups in Kibale National Park, Uganda, as well as microsatellite genotyping of these and two other neighbouring groups. We created a statistical model to examine the observational data and used dyadic relatedness values within and among groups to analyse the genetic data. Analyses of observational and genetic data both supported the conclusion that males typically disperse from their natal groups and often transfer into nearby groups and probably beyond. Both data types also supported the conclusion that females are more philopatric than males but provided somewhat conflicting evidence about the extent of female philopatry. Observational data suggested that female dispersal is rare or nonexistent and transfers into neighbouring groups do not occur, but genetic data revealed numerous pairs of closely related adult females among neighbouring groups. Only by combining both data types were we able to understand the complexity of sex-biased dispersal patterns in guerezas and the processes that could explain our seemingly conflicting results. We suggest that the data are compatible with a scenario of group dissolution prior to the start of this study, followed by female transfers into different neighbouring groups.     

Hierarchical analysis of population genetic structure in the monogynous ant Cataglyphis cursor using microsatellite and mitochondrial DNA markers

Despite having winged queens, female dispersal in the monogynous ant Cataglyphis cursor is likely to be restricted because colonies reproduce by fission. We investigated the pattern of population genetic structure of this species using eight microsatellite markers and a mitochondrial DNA (mtDNA) sequence, in order to examine the extent of female and nuclear gene flow in two types of habitat. Sampling was carried out at a large spatial scale (16 sites from 2.5 to 120 km apart) as well as at a fine spatial scale (two 4.5-km transects, one in each habitat type). The strong spatial clustering of mtDNA observed at the fine spatial scale strongly supported a restricted effective female dispersal. In agreement, patterns of the mtDNA haplotypes observed at large and fine spatial scales suggested that new sites are colonized by nearby sites. Isolation by distance and significant nuclear genetic structure have been detected at all the spatial scales investigated. The level of local genetic differentiation for mitochondrial marker was 15 times higher than for the nuclear markers, suggesting differences in dispersal pattern between the two sexes. However, male gene flow was not sufficient to prevent significant nuclear genetic differentiation even at short distances (500 m). Isolation-by-distance patterns differed between the two habitat types, with a linear decrease of genetic similarities with distance observed only in the more continuous of the two habitats. Finally, despite these low dispersal capacities and the potential use of parthenogenesis to produce new queens, no signs of reduction of nuclear genetic diversity was detected in C. cursor populations.     

Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus)

In most mammals males usually disperse before breeding, while females remain in their natal group or area. However, in odontocete cetaceans behavioural and/or genetic evidence from populations of four species indicate that both males and females remain in their natal group or site. For coastal resident bottlenose dolphins field data suggest that both sexes are philopatric to their natal site. Assignment tests and analyses of relatedness based on microsatellite markers were used to investigate this hypothesis in resident bottlenose dolphins, Tursiops aduncus, from two small coastal populations of southeastern Australia. Mean corrected assignment and mean relatedness were higher for resident females than for resident males. Only 8% of resident females had a lower probability than average of being born locally compared to 33% of resident males. Our genetic data contradict the hypothesis of bisexual philopatry to natal site and suggest that these bottlenose dolphins are not unusual amongst mammals, with females being the more philopatric and males the more dispersing sex.     

Assisted dispersal and reproductive success in an ant species with matchmaking

Workers of the ant Cardiocondyla elegans drop female sexuals into the nest entrance of other colonies to promote outbreeding with unrelated, wingless males. Corroborating the results from previous years, we document that carrier and carried female sexuals are typically related and that the transfer initially occurs mostly from their joint natal colonies to unrelated colonies. Female sexuals mate multiply with up to seven genetically distinguishable males. Contrary to our expectation, the colony growth rate of multiple‐mated and outbred female sexuals was lower than that of inbred or single‐mated females, leading to the question of why female sexuals mate multiply at all. Despite the obvious costs, multiple mating might be a way for female sexuals to “pay rent” for hibernation in an alien nest. We argue that in addition to evade inbreeding depression from regular sibling mating over many generations, assisted dispersal might also be a strategy for minimizing the risk of losing all reproductive investment when nests are flooded in winter.     

Fine-scale population genetic structure in a fission-fusion society

Nonrandom patterns of mating and dispersal create fine-scale genetic structure in natural populations — especially of social mammals — with important evolutionary and conservation genetic consequences. Such structure is well-characterized for typical mammalian societies; that is, societies where social group composition is stable, dispersal is male-biased, and males form permanent breeding associations in just one or a few social groups over the course of their lives. However, genetic structure is not well understood for social mammals that differ from this pattern, including elephants. In elephant societies, social groups fission and fuse, and males never form permanent breeding associations with female groups. Here, we combine 33 years of behavioural observations with genetic information for 545 African elephants ( Loxodonta africana ), to investigate how mating and dispersal behaviours structure genetic variation between social groups and across age classes. We found that, like most social mammals, female matrilocality in elephants creates co-ancestry within core social groups and significant genetic differentiation between groups (Φ_ST = 0.058). However, unlike typical social mammals, male elephants do not bias reproduction towards a limited subset of social groups, and instead breed randomly across the population. As a result, reproductively dominant males mediate gene flow between core groups, which creates cohorts of similar-aged paternal relatives across the population. Because poaching tends to eliminate the oldest elephants from populations, illegal hunting and poaching are likely to erode fine-scale genetic structure. We discuss our results and their evolutionary and conservation genetic implications in the context of other social mammals.     

Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis

Using four highly polymorphic microsatellite markers (12-28 alleles), we gentoyped workers from 63 colonies of Pogonomyrmex occidentalis. Colonies have a single, multiply mated queen, and an average number of 6.3 patrilines per colony. Colony growth was measured over an 8-year period in the study population. Intracolonial relatedness and colony growth are correlated negatively, indicating a substantial fitness benefit to multiple mating.     

Tests for sex-biased dispersal using bi-parentally inherited genetic markers

Understanding why dispersal is sex-biased in many taxa is still a major concern in evolutionary ecology. Dispersal tends to be male-biased in mammals and female-biased in birds, but counter-examples exist and little is known about sex bias in other taxa. Obtaining accurate measures of dispersal in the field remains a problem. Here we describe and compare several methods for detecting sex-biased dispersal using bi-parentally inherited, codominant genetic markers. If gene flow is restricted among populations, then the genotype of an individual tells something about its origin. Provided that dispersal occurs at the juvenile stage and that sampling is carried out on adults, genotypes sampled from the dispersing sex should on average be less likely (compared to genotypes from the philopatric sex) in the population in which they were sampled. The dispersing sex should be less genetically structured and should present a larger heterozygote deficit. In this study we use computer simulations and a permutation test on four statistics to investigate the conditions under which sex-biased dispersal can be detected. Two tests emerge as fairly powerful. We present results concerning the optimal sampling strategy (varying number of samples, individuals, loci per individual and level of polymorphism) under different amounts of dispersal for each sex. These tests for biases in dispersal are also appropriate for any attribute (e.g. size, colour, status) suspected to influence the probability of dispersal. A windows program carrying out these tests can be freely downloaded from http://www.unil.ch/izea/softwares/fstat.html     

Dispersal, philopatry and intergroup relatedness: fine-scale genetic structure in the white-breasted thrasher, Ramphocinclus brachyurus

Dispersal is a fundamental process influencing evolution, social behaviour, and the long-term persistence of populations. We use both observational and genetic data to investigate dispersal, kin-clustering and intergroup relatedness in the white-breasted thrasher, Ramphocinclus brachyurus, a cooperatively breeding bird that is globally endangered. Mark-resighting data suggested sex-biased dispersal, with females dispersing over greater distances while males remained philopatric. Accordingly, spatial autocorrelation analysis showed highly significant fine-scale genetic structure among males, but not among females. This fine-scale genetic structuring of the male population resulted in very high levels of relatedness between dominant males at neighbouring nests, similar to that seen within cooperative groups in many species where kin selection is cited as a cause of cooperation. By implication, between-group as well as within-group cooperation may be important, potentially creating a feedback loop in which short-distance dispersal by males leads to the formation of male kin clusters that in turn facilitate nepotistic interactions and favour further local recruitment. The strength of spatial autocorrelation, as measured by the autocorrelation coefficient, r, was approximately two to three times greater than that reported in previous studies of animals. Relatively short dispersal distances by both males and females may have a negative impact on the white-breasted thrasher's ability to colonize new areas, and may influence the long-term persistence of isolated populations. This should be taken into account when designating protected areas or selecting sites for habitat restoration.     

Macro- and microgeographic genetic structure in an ant species with alternative reproductive tactics in sexuals

The genetic structure of social insect populations is influenced by their social organization and dispersal modes. The ant Hypoponera opacior shows diverse reproductive behaviours with regular cycles of outbreeding via winged sexuals and inbreeding via within-nest mating wingless sexuals that reproduce by budding. This unusual life cycle should be reflected in the genetic population structure, and we studied this on different scales using microsatellites. On a macrogeographic scale, populations were considerably structured and migration rates within the Chiricahuas were higher than those in between mountain ranges. On a local scale, our analyses revealed population viscosity through dependent colony foundation and a high genetic diversity with a multicolonial structure. The latter was also evident from recognition trials revealing consistent aggression between non-nestmates. Within-nest matings led to high inbreeding coefficients. Finally, the observed seasonal changes in relatedness can be explained by variation in queen number and differential dispersal of the two reproductive morphs.     

Population genetic structure and male-biased dispersal in the queenless ant Diacamma cyaneiventre

In this study we investigated the population genetic structure of the queenless ant Diacamma cyaneiventre. This species, lacking winged queens, is likely to have a restricted female dispersal. We used both mitochondrial and microsatellite markers to assess the consequence of such restricted female dispersal at three geographical scales: within a given locality (< 1 km), between localities within a given region (< 10 km) and between regions (> 36 km). Within a locality, a strong population structure was observed for mitochondrial DNA (mtDNA) whereas weak or nonexistent population genetic structure was observed for the microsatellites (around 5% of the value for mtDNA). Male gene flow was estimated to be about 20-30 times higher than female gene flow at this scale. At a larger spatial scale, very strong genetic differentiation for both markers was observed between localities - even within a single region. Female dispersal is nonexistent at these scales and male dispersal is very restricted, especially between regions. The phylogeographical structure of the mtDNA haplotypes as well as the very low genetic diversity of mtDNA within localities indicate that new sites are colonized by a single migration event from adjacent localities, followed by successive colony fissions. These patterns of genetic variability and differentiation agree with what is theoretically expected when colonization events are kin-structured and when, following colonization, dispersion is mainly performed by males.     

Mating frequency and genetic structure of the Argentine ant Linepithema humile

The nest and population genetic structures of the Argentine ant, Linepithema humile were investigated using eight microsatellite loci. Genotypes of the sperm from spermathecae of 87 queens were consistent with all queens being singly inseminated. The probability of a double mating remaining undetected was low (0.012) suggesting that no queens or only a very low proportion mate multiply. The relatedness between the queens and their mates was negative (R = -0.164 +/- 0.044) and significantly different to zero (P = 0.020). However, the high negative relatedness value was caused by a significant allele frequency difference between the sexes at a single locus (Lhum-28). When this locus was removed from the analyses, the relatedness was not significantly different from zero (R = 0.013 +/- 0.050, P = 0.812). Analysis of 10 nests revealed that the genetic differentiation among nests was weak (FST = 0.003) and not distinguishable from zero (P = 0.468). Similarly, the overall relatedness among nestmate females was not significantly different from zero (R = 0.007 +/- 0.018, P = 0.706). These results are consistent with the lack of distinct nest boundaries and the large number of queens per nest in the population studied. Although mating takes place inside the nest, the inbreeding coefficient was close to zero (F = 0.007 +/- 0.025, P = 0.786). Overall, these data indicate substantial local gene flow mediated by movement of reproductives among colonies.     

Mating frequency and genetic relatedness of workers in the hornet Vespa analis (Hymenoptera: Vespidae)

Mating frequency of Vespa analis queens and the genetic relatedness of their workers was analyzed by DNA microsatellite genotyping. Of 20 colonies studied, 18 had a queen inseminated by a single male and two had queens each inseminated by two males. The estimated effective number of matings was 1.05 ± 0.037 (mean ± SE), with 75–85% of the offspring of the two multiply mated queens sired by a single male. The pedigree relatedness between nestmate workers averaged over the 20 colonies was estimated to be 0.74 ± 0.008, almost identical to the predicted value of 0.75 for colonies headed by a singly mated queen. Multiple matrilines; that is, the presence of workers not related to the current queens, were detected in six colonies, suggesting that queen replacement occurred via usurpation of the founding queens in these six colonies. These results demonstrate that the kin structure of V. analis is similar to that reported in other vespid species.     

Fine-scale spatial genetic structure and gene dispersal in Silene latifolia

Plants are sessile organisms, often characterized by limited dispersal. Seeds and pollen are the critical stages for gene flow. Here we investigate spatial genetic structure, gene dispersal and the relative contribution of pollen vs seed in the movement of genes in a stable metapopulation of the white campion Silene latifolia within its native range. This short-lived perennial plant is dioecious, has gravity-dispersed seeds and moth-mediated pollination. Direct measures of pollen dispersal suggested that large populations receive more pollen than small isolated populations and that most gene flow occurs within tens of meters. However, these studies were performed in the newly colonized range (North America) where the specialist pollinator is absent. In the native range (Europe), gene dispersal could fall on a different spatial scale. We genotyped 258 individuals from large and small (15) subpopulations along a 60 km, elongated metapopulation in Europe using six highly variable microsatellite markers, two X-linked and four autosomal. We found substantial genetic differentiation among subpopulations (global F_ST=0.11) and a general pattern of isolation by distance over the whole sampled area. Spatial autocorrelation revealed high relatedness among neighboring individuals over hundreds of meters. Estimates of gene dispersal revealed gene flow at the scale of tens of meters (5–30 m), similar to the newly colonized range. Contrary to expectations, estimates of dispersal based on X and autosomal markers showed very similar ranges, suggesting similar levels of pollen and seed dispersal. This may be explained by stochastic events of extensive seed dispersal in this area and limited pollen dispersal.     

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

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

Inferring colonization history from analyses of spatial genetic structure within populations of Pinus strobus and Quercus rubra

Many factors interact to determine genetic structure within populations including adult density, the mating system, colonization history, natural selection, and the mechanism and spatial patterns of gene dispersal. We examined spatial genetic structure within colonizing populations of Quercus rubra seedlings and Pinus strobus juveniles and adults in an aspen-white pine forest in northern Michigan, USA. A 20-year spatially explicit demographic study of the forest enables us to interpret the results in light of recent colonization of the site for both species. We assayed 217 Q. rubra seedlings and 171 P. strobus individuals at 11 polymorphic loci using nine allozyme systems. Plant genotypes and locations were used in an analysis of spatial genetic structure. Q. rubra and P. strobus showed similar observed levels of heterozygosity, but Q. rubra seedlings have less heterozygosity than expected. Q. rubra seedlings show spatial genetic clumping of individuals on a scale to 25 m and levels of genetic relatedness expected from the clumped dispersion of half-siblings. In contrast, P. strobus has low levels of genetic relatedness at the smallest distance class and positive spatial genetic structure at scales < 10 m within the plot. The low density of adult Q. rubra outside the study plot and limited, spatially clumped rodent dispersal of acorns is likely responsible for the observed pattern of spatial genetic structure and the observed heterozygote deficit (i.e. a Wahlund effect). We attribute weaker patterns observed in P. strobus to the longer dispersal distance of seeds and the historical overlap of seed shadows from adults outside of the plot coupled with the overlap of seed shadows from younger, more recently established reproductive adults. The study demonstrates the utility of long-term demographic data in interpreting mechanisms responsible for generating contemporary patterns of genetic structure within populations.     

Reproductive conflicts in polyandrous and polygynous ant Formica sanguinea

The occurrence of multiple reproductives within an ant colony changes the balance between indirect fitness benefits and reproductive competition. We test whether the number of matings by an ant queen (polyandry) correlates negatively with the number of reproductive queens in the colony (polygyny), whether the patrilines and matrilines differ in their contribution to the sexual and worker progeny and whether there is an overall reproductive skew. For these aims, we genotyped both worker and sexual offspring from colonies of the ant Formica sanguinea in three populations. Most colonies were monogynous, but eight (11%) were polygynous with closely related queens. Most queens in the monogynous colonies (86%) had mated with multiple males. The effective paternity was lower than the actual number of mates, and the paternity skew was significant. Furthermore, in some monogynous colonies, the patrilines were differently represented in the worker pupae and sexual pupae produced at the same time. Likewise, the matrilines in polygynous colonies were differently present in worker pupae and male offspring. The effective number of matings by a queen was significantly lower in polygynous colonies (mean m_e = 1.68) than in monogynous colonies (means 2.06–2.61). The results give support to the hypotheses that polyandry and polygyny are alternative breeding strategies and that reproductive competition can lead to different representation of patrilines and matrilines among the sexual and worker broods.     

Social structure in migrating humpback whales (Megaptera novaeangliae)

Although largely solitary, humpback whales exhibit a number of behaviours where individuals co-operate with one another, for example during bubble net feeding. Such cases could be due to reciprocal altruism brought on by exceptional circumstances, for example the presence of abundant shoaling fish. An alternative explanation is that these behaviours have evolved through kin selection. With little restriction to either communication or movement, diffuse groups of relatives could maintain some form of social organization without the need to travel in tight-nit units. To try to distinguish between these hypotheses, we took advantage of the fact that migrating humpback whales often swim together in small groups. If kin selection is important in humpback whale biology, these groups should be enriched for relatives. Consequently, we analysed biopsy samples from 57 groups of humpback whales migrating off Eastern Australia in 1992. A total of 142 whales were screened for eight microsatellite markers. Mitochondrial DNA sequences (371 bp) were also used to verify and assist kinship identification. Our data add support to the notion that mothers travel with their offspring for the first year of the calf's life. However, beyond the presence of mother-calf/yearling pairs, no obvious relatedness pattern was found among whales sampled either in the same pod or on the same day. Levels of relatedness did not vary between migratory phases (towards or away from the breeding ground), nor between the two sexes considered either overall or in the north or south migrations separately. These findings suggest that, if any social organization does exist, it is formed transiently when needed rather than being a constant feature of the population, and hence is more likely based on reciprocal altruism than kin selection.     

Recruitment, kin and the spatial genetic structure of a caddisfly Plectrocnemia conspersa in a southern English stream

1. Our objectives were to examine small‐scale patterns in oviposition and genetic relatedness in a population of the stream‐dwelling caddis Plectrocnemia conspersa and, in particular, to look for any evidence of the spatial proximity of close kin and, therefore, ‘patchy recruitment’. 2. In order to examine the distribution of related larvae at the beginning of the aquatic phase, we searched the stream for egg masses. Spatially and temporally structured samples of larvae were then collected from the stream over four sample dates within one generation. The genetic relatedness of these field‐collected larvae, estimated using six polymorphic microsatellite loci, was subsequently compared with that of larvae reared from individual egg masses in the laboratory. 3. Egg masses were laid in clusters or ‘hot spots’ along the stream. The mean relatedness coefficient within reared egg masses ranged from 0.327 to 0.525, and differed significantly from that estimated for the population as a whole (0.070), indicating that the markers were sufficiently powerful to identify groups of siblings. Each egg mass was likely to be the progeny of one father, although the possibility of a small contribution from a second male could not be excluded for a few masses. 4. Mean relatedness within the spatially structured groups of larvae in the stream, even those in close proximity to each other, did not differ from the background population level estimate, suggesting that siblings disperse away from each other very quickly and that kin structure does not persist over time. 5. Changes in spatial genetic structure late in the larval life indicated that neighbouring larvae were less closely related than the population overall, possibly suggesting some direct or indirect means of avoiding kin when approaching the onset of pupation. 6. Our counts of egg masses suggested that survival through the egg stage and early larval life was apparently very high (>50%) for a non‐social insect, and may be a consequence of the colonial net that is briefly occupied by first instar larvae. 7. The number of egg masses laid in the stream (approximately 400 in the sample year), the lack of a spatial genetic structure showing evidence of families even early in larval life, and the high survival of eggs and early instar larvae, all refute the ‘patchy recruitment hypothesis’ for this species.