Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds

In cooperatively breeding species, restricted dispersal of offspring leads to clustering of closely related individuals, increasing the potential both for indirect genetic benefits and inbreeding costs. In apostlebirds (Struthidea cinerea), philopatry by both sexes results in the formation of large (up to 17 birds), predominantly sedentary breeding groups that remain stable throughout the year. We examined patterns of relatedness and fine-scale genetic structure within a population of apostlebirds using six polymorphic microsatellite loci. We found evidence of fine-scale genetic structure within the study population that is consistent with behavioural observations of short-distance dispersal, natal philopatry by both sexes and restricted movement of breeding groups between seasons. Global F(ST) values among breeding groups were significantly positive, and the average level of pairwise relatedness was significantly higher for individuals within groups than between groups. For individuals from different breeding groups, geographical distance was negatively correlated with pairwise relatedness and positively correlated with pairwise F(ST). However, when each sex was examined separately, this pattern was significant only among males, suggesting that females may disperse over longer distances. We discuss the potential for kin selection to influence the evolution and maintenance of cooperative breeding in apostlebirds. Our results demonstrate that spatial genetic structural analysis offers a useful alternative to field observations in examining dispersal patterns of cooperative breeders.     

Directed dispersal of mistletoe (Plicosepalus acaciae) by Yellow-vented Bulbuls (Pycnonotus xanthopygos)

We studied avian dispersal of seeds from the hemiparasitic mistletoe Plicosepalus acaciae (Loranthaceae) to its tree hosts Acacia raddiana and A. tortilis in the Syrian–African Rift (Arava) valley, Israel. The Yellow-vented Bulbul (Pycnonotus xanthopygos) was the sole avian visitor observed feeding on mistletoe fruits. Bulbuls consumed mistletoe fruits whenever they were available, but the fruits only constituted a significant portion of the diet (71% of foraging attempts) when they were most abundant. These birds are potentially good dispersal vectors of P. acaciae because they swallowed the fruit whole and defecated viable seeds that were covered in a viscid pulp, which allowed the seeds to adhere to substrates when voided. In addition, bulbuls spent a large proportion (66–93%) of total observation time perched in Acacia trees, allowing for directed dispersal. Ephemeral river valleys (wadis) with high mistletoe infection were adjacent to those containing no infections, demonstrating that mistletoe dispersal is common within, but not among wadis. This is consistent with the flight behaviour in bulbuls, which do not typically move among wadis. We combined data on bulbul movements between Acacia trees with transit times of mistletoe seeds to create a hypothetical seed shadow as a function of distance from the parent mistletoe plant. Because they are directed dispersers, the movement patterns of bulbuls may explain the current distribution of P. acaciae in the Arava valley.     

The absence of sex-biased dispersal in the cooperatively breeding grey-crowned babbler

1. Cooperatively breeding birds are thought to be especially vulnerable to habitat fragmentation, in part because dispersal is typically restricted for one sex, increasing the likelihood of inbreeding. Knowledge of dispersal is essential to conservation efforts, but is often hampered by our inability to measure its frequency and distance when dispersal is infrequent and difficult to observe. 2. Disrupted dispersal is a purported cause of decline in the Australian grey-crowned babbler (Pomatostomus temporalis). Both sexes of offspring delay dispersal for up to several years to help parents raise subsequent broods, yet little else is known about the dispersal of this cooperatively breeding woodland bird. 3. As both sexes appear to help, but only male helpers boost fledgling production, we hypothesized that males would be the more philopatric sex in this species, and that female grey-crowned babblers would disperse over greater distances. 4. To ensure reliable determination of sex and minimize bias towards detecting short-distance dispersal events, we combined molecular-based sexing and analyses of population genetic structure using polymorphic microsatellite loci with observational data obtained over multiple field seasons. 5. Observations of banded birds showed only infrequent fission of groups or short-distance dispersal (mean=854 m), but no apparent sex-bias in these patterns. 6. There was significant genetic differentiation between social groups, but not between the sexes. Spatial genetic autocorrelation analysis of breeders revealed a random distribution of genotypes across the study area for both sexes. Thus, contrary to expectations, we found no genetic evidence for restricted dispersal or for sex-biased dispersal over the 85-km scale of this study, indicating that effective dispersal occurs over greater distances and more frequently than recoveries of banded birds indicated. 7. We conclude that while constraints on independent breeding encourage high rates of philopatry, incest avoidance nonetheless drives high rates of dispersal by both sexes. In fragmented habitat, the dispersal dynamics of this cooperatively breeding species are unlikely to render them particularly vulnerable to genetic consequences such as inbreeding, but may lead to increased group dissolution.     

The fitness consequences of kin-biased dispersal in a cooperatively breeding bird

Cooperative alliances among kin may not only lead to indirect fitness benefits for group-living species, but can also provide direct benefits through access to mates or higher social rank. However, the immigrant sex in most species loses any potential benefits of living with kin unless immigrants disperse together or recruit relatives into the group in subsequent years. To look for evidence of small subgroups of related immigrants within social groups (kin substructure), we used microsatellites to assess relatedness between immigrant females of the cooperatively breeding superb starling, Lamprotornis superbus. We determined how timing of immigration led to kin subgroup formation and if being part of one influenced female fitness. Although mean relatedness in groups was higher for males than females, 26% of immigrant females were part of a kin subgroup with a sister. These immigrant sibships formed through kin recruitment across years more often than through coalitions immigrating together in the same year. Furthermore, females were more likely to breed when part of a kin subgroup than when alone, suggesting that female siblings form alliances that may positively influence their fitness. Ultimately, kin substructure should be considered when determining the role of relatedness in the evolution of animal societies.     

Circus pallidus bei Danzig erlegt

Ohne Zusammenfassung     

Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish

African Great Lake cichlid populations are divided into thousands of genetic subpopulations. The low gene flow between these subpopulations is thought to result from high degrees of natal philopatry, heavy predation pressure, and a patchy distribution of preferred habitats. While predation pressure and habitat distribution are fairly straightforward to assess, data on dispersal distances and rates are scarce. In fishes, direct observations of dispersal events are unlikely, but dispersal can be studied using molecular markers. Using seven microsatellite loci, we examined dispersal in the cooperatively breeding cichlid fish, Neolamprologus pulcher. As this species is found in well-defined groups clustered into subpopulations, we could assess dispersal on a narrow (within subpopulation) and broad (between subpopulation) scale. While fish were generally more related to others in their own subpopulation than they were to fish from other subpopulations, large males diverged from this pattern. Large males were more related to other large males from different subpopulations than they were to large males from their own subpopulation, suggesting more frequent dispersal by large males. Across subpopulations, relatedness between large males was higher than the relatedness among large females; this pattern was not detected in small males and small females. Within a subpopulation, individuals appeared to be preferentially moving away from relatives, and movement was unrestricted by the physical distance between groups. Our results highlight the importance of examining multiple spatial scales when studying individual dispersal biases.     

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

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

Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal

Hamilton demonstrated that the evolution of cooperative behaviour is favoured by high relatedness, which can arise through kin discrimination or limited dispersal (population viscosity). These two processes are likely to operate with limited overlap: kin discrimination is beneficial when variation in relatedness is higher, whereas limited dispersal results in less variable and higher average relatedness, reducing selection for kin discrimination. However, most empirical work on eukaryotes has focused on kin discrimination. To address this bias, we analysed how kin discrimination and limited dispersal interact to shape helping behaviour across cooperatively breeding vertebrates. We show that kin discrimination is greater in species where the: (i) average relatedness in groups is lower and more variable; (ii) effect of helpers on breeders reproductive success is greater; and (iii) probability of helping was measured, rather than the amount of help provided. There was also an interaction between these effects with the correlation between the benefits of helping and kin discrimination being stronger in species with higher variance in relatedness. Overall, our results suggest that kin discrimination provides a route to indirect benefits when relatedness is too variable within groups to favour indiscriminate cooperation.     

Hormonal influences on natal dispersal in free-living Belding's ground squirrels (Spermophilus beldingi)

Preliminary identification of the physiological causes of natal dispersal in two populations of free-living Belding's ground squirrels (Spermophilus beldingi) was attempted in the Sierra Nevada of California. Two competing hypotheses, each suggesting a different endocrinological cause for natal dispersal in this species were tested. Data collected by observation, trapping, and telemetry during three field seasons (1979–1981) contradict predictions of the hypothesis that concurrent, high levels of circulating gonadal steroids cause natal dispersal. Rather the data suggest that perinatal exposure to androgen subsequently results in dispersal of treated individuals. The hormone may promote dispersal behavior through its mediating effects on juveniles' exploratory and social behaviors, and on their responsiveness to frightening stimuli. Possible interactions of endocrine mechanisms with other proximal and ultimate causes of dispersal are discussed.     

Effects of habitat fragmentation on the timing of Crested Tit Parus cristatus natal dispersal

Crested Tit Parus cristatus young from first broods dispersed 1 week later if they were born in small isolated pine plots ('habitat fragments') compared with individuals in a large pine forest ('continuous habitat'). This delay in dispersal was caused by an extended period between fledging and dispersal. In second broods, the delay was even longer due to the interbrood interval being 9 days longer in habitat fragments. As nestlings in habitat fragments had a lower body-mass, and age at dispersal was negatively correlated with nestling body-mass within each nest, the postponed dispersal from fragments might be explained partly by a lower body-mass. Alternatively, postponed dispersal from fragments could result from a barrier effect caused by reluctance to cross inhospitable habitat.
Immigration by young from first broods into habitat fragments was delayed by approximately 3 weeks, and proportionally more second brood emigrants were recovered in this type of habitat. These results are in agreement with the hypothesis that fragments are second-choice habitat. Early immigrants into continuous habitat had a higher probability of settlement in winter flocks compared with late ones, independent of condition or age. Therefore, Crested Tits born in habitat fragments probably have a lower chance of settling in first-choice habitat.     

Experimentally increased food resources in the natal territory promote offspring philopatry and helping in cooperatively breeding carrion crows

Kin-based societies, where families represent the basic social unit, occur in a relatively small number of vertebrate species. In the majority of avian kin societies, families form when offspring prolong their association with the parents on the natal territory. Therefore, the key to understanding the evolution of families in birds is to understand natal philopatry (i.e. the tendency to remain on the natal territory). It has been shown that, within populations, the strength of the association between parents and offspring (i.e. family stability) increases when offspring dispersal is constrained by external environmental factors, but it is unclear whether and how family wealth influences juvenile dispersal decisions. Here, we show that young carrion crows (Corvus corone corone) from territories that were food-supplemented year-round were more philopatric and more likely to help at their family's nest than the unfed ones. The results suggest that offspring philopatry and helping behaviour are influenced by the quality of 'home' and that the availability of food resources positively affects the cohesion of the family.     

Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid

Environmental conditions are thought to be responsible for the extent and benefits of cooperative breeding in many animal societies, but experimental tests are scarce. We manipulated predator pressure in the cooperatively breeding cichlid Neolamprologus pulcher in Lake Tanganyika, where predators have been suggested to influence helper and breeder survival, helper dispersal and group reproductive success. We varied the type and intensity of predation by releasing medium, large, or no predators inside large underwater cages enclosing two or three group territories. Helper and breeder survival, helper dispersal and group reproductive success decreased from the control, to the medium- and large-predator treatments. These effects were modified by helper body size and the number of adults protecting the group from predators, supporting the 'group augmentation hypothesis'. Predators forced helpers to stay closer to, and spend more time inside, protective shelters. The results demonstrate the importance of predators for group living in this species, and support the 'ecological constraints hypothesis' of cooperative breeding, in the sense that subordinates stay at home rather than leave and breed independently under the risk of predation.