Delayed dispersal as a route to breeding: territorial inheritance, safe havens, and ecological constraints

The relative roles of ecological constraints, the benefits of philopatry, and the role of life history continue to be debated in the evolution of natal philopatry and cooperative breeding. We compare three routes to breeding: departing to search for territories as a floater, staying and queuing to inherit the natal territory, or queuing and eventually shifting to a neighboring vacancy. Our model assumed a dominance-structured population. It quantifies the benefits of philopatry for varying-rank subordinates and contrasts it against the benefit of dispersal. We apply the model to data on Siberian jay Perisoreus infaustus, a species in which retained offspring do not help at the nest. The results indicate that territorial inheritance plays a small role in this species (presumably due to inbreeding avoidance), and territory acquisition is less constrained for dispersing than philopatric offspring. Nevertheless, small family groups-one or, at the most, two same-sex queuers-are predicted to form because philopatric offspring gain nepotistic benefits that improve their survival. This fits with data on group sizes and supports the idea of the natal territory as a safe haven for waiting for breeding opportunities. We also discuss our predictions in the light of ecological constraints and clarify recent confusingly different predictions on the role of habitat saturation as an explanation for delayed dispersal and cooperative breeding. We argue that "ecological constraint" is too wide a term to yield useful predictive power and that it is more appropriate to examine the consequences of specific life-history traits on the success of dispersers.     

Delayed dispersal and prolonged brood care in a family‐living beetle

Delayed juvenile dispersal is an important prerequisite for the evolution of family‐based social systems, such as cooperative breeding and eusociality. In general, young adults forego dispersal if there are substantial benefits to remaining in the natal nest and/or the likelihood of dispersing and breeding successfully is low. We investigate some general factors thought to drive delayed juvenile dispersal in the horned passalus beetle, a family‐living beetle in which young adults remain with their families in their natal nest for several months before dispersing. Fine‐scale population genetic structure indicated high gene flow between nest sites, suggesting that constraints on mobility are unlikely to explain philopatry. Young adults do not breed in their natal log and likely disperse before reaching breeding age, suggesting that they do not gain direct reproductive benefits from delayed dispersal. We also examined several ways in which parents might incentivize delayed dispersal by providing prolonged care to adult offspring. Although adult beetles inhibit fungal growth in the colony by manipulating both the nest site and deceased conspecifics, this is unlikely to be a major explanation for family living as both parents and adult offspring seem capable of controlling fungal growth. Adult offspring that stayed with their family groups also neither gained more mass nor experienced faster exoskeleton development than those experimentally removed from their families. The results of these experiments suggest that our current understanding of the factors underlying prolonged family living may be insufficient to explain delayed dispersal in at least some taxa, particularly insects.     

The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus)

It is widely accepted that natal philopatry is a prerequisite for the evolution of sociality. The life-history hypothesis maintains that longevity of adults results in extended territory tenure and thus limits breeding vacancies for offspring, which makes natal philopatry more likely. Here, we tested the importance of longevity for natal philopatry in females of a basal primate, the grey mouse lemur (Microcebus murinus). This species is regarded as being solitary due to its foraging habits but while males disperse, female offspring in this species forgo dispersal and form long-term sleeping groups with their mothers. We tested whether high adult survival could be a cause for natal philopatry of female offspring. In addition, we assessed costs and benefits associated with space sharing between mothers and daughters and whether mothers actively increase survival of daughters by beqeauthal of territories, information transfer about resources or thermoregulation. Contrary to our predictions, adult females had low-survival rates. Space sharing appeared to improve survival of both, mothers and daughters. This could be a result of information transfer about sleeping sites and thermoregulatory benefits. Our results cast doubt on the idea that longevity predisposes species for social traits and provide support for benefits of philopatry.     

History,environment and social behaviour: experimentally induced cooperative breeding in the carrion crow

Kin-based cooperative breeding, where grown offspring delay natal dispersal and help their parents to rear new young, has a long history in some avian lineages. Family formation and helping behaviour in extant populations may therefore simply represent the retention of ancestral features, tolerated under current conditions, rather than a current adaptive process driven by environmental factors. Separating these two possibilities challenges evolutionary biologists because of the tight coupling that normally exists between phylogeny and the environmental distribution of species and populations. The carrion crow Corvus corone corone, which exhibits extreme interpopulational variation in the extent of cooperative breeding, with populations showing no delayed dispersal and helping at all, provides a unique opportunity for an experimental approach. Here we show that offspring of non-cooperative carrion crows from Switzerland will remain on the natal territory and express helping behaviour when raised in a cooperative population in Spain. When we transferred carrion crow eggs from Switzerland to Spain, five out of six transplanted juveniles delayed dispersal, and two of those became helpers in the following breeding season. Our results provide compelling experimental evidence of the causal relationship between current environmental conditions and expression of cooperative behaviour.     

Why offspring delay dispersal: experimental evidence for a role of parental tolerance

Approximately 3% of all bird species live in families based on a prolonged parent-offspring association. Formation of family groups often appears to be associated with various constraints on the possibilities of independent reproduction for the offspring. However, delayed dispersal is not the only alternative for offspring that defer reproduction. To account for the formation of a family group it is also necessary to explain why non-dispersing offspring forego the alternative options to join other groups as 'extra birds' or to become 'floaters' and roam between territories. We removed fathers from Siberian jay Perisoreus infaustus family groups to test the proposal that nepotistic parental tolerance gives the natal territory a special value for the offspring, which they cannot find elsewhere and that makes them stay. In this species, parents are more tolerant of their retained offspring than towards immigrant extra birds. In response to the removal of fathers, retained offspring dispersed, whereas there was no similar response among the unrelated extra birds. Retained offspring, however, left only after despotic immigrant alpha-males replaced removed fathers, indicating that the presence of fathers is an essential motive for offspring to delay their dispersal. By blocking immigrant and unrelated males from becoming alpha-males and by being tolerant themselves, fathers provide a 'safe haven' in the natal territory where retained offspring can avail themselves of available resources without any, or only mild, competitive interference.     

Social and ecological influences on dispersal and philopatry in the plateau pika (Ochotona curzoniae)

Benefits and costs of dispersal and philopatry of the socialplateau pika (Ochotona curzoniae) were studied on the Tibetanplateau for 3 years. Although short-lived, plateau pikas livein cohesive family groups that occupy burrow systems in sedgemeadow habitat Most (57.8%) plateau pikas were philopatric,and dispersal movements were extremely restricted. No juvenilefemales or adult pikas moved more than two family ranges betweenyears; the greatest observed dispersal distances were by twojuvenile males that moved five family ranges from the familyof their birth. Traversing unfamiliar habitat was not a costof pika dispersal because most dispersers settled in familiesthat they could easily visit before dispersal. Dispersal movementsappeared to result in equalization of density among pika families,an expected result if competition for environmental resourcesinfluenced dispersal. Males did not disperse to gain advantagesin competition for mates, as evidenced by their moving to familieswith significantly fewer females. Females, however, moved tofamilies with significantly more males. Males provide abundantpaternal care, and significantly more offspring per female survivedto become adults from families with more adult males per adultfemale. Evidence concerning the influence of inbreeding avoidanceon natal dispersal was indirect. Some males exhibited natalphilopatry; thus some families had opportunity for dose inbreeding.Males and females that dispersed had no opposite-sex relativesin their new families. Philopatric pikas may have benefitedby remaining in families that exhibited low local densities,and philopatric females might have benefited from social cooperationwith relatives.     

Dispersal,philopatry, and the role of fission‐fusion dynamics in bottlenose dolphins

In this quantitative study of locational and social dispersal at the individual level, we show that bottlenose dolphins (Tursiops sp.) continued to use their natal home ranges well into adulthood. Despite substantial home range overlap, mother–offspring associations decreased after weaning, particularly for sons. These data provide strong evidence for bisexual locational philopatry and mother–son avoidance in bottlenose dolphins. While bisexual locational philopatry offers the benefits of familiar social networks and foraging habitats, the costs of philopatry may be mitigated by reduced mother–offspring association, in which the risk of mother–daughter resource competition and mother–son mating is reduced. Our study highlights the advantages of high fission–fusion dynamics and longitudinal studies, and emphasizes the need for clarity when describing dispersal in this and other species.     

Processes at the origin of similarities in dispersal behaviour among siblings

Processes which generate natal dispersal are largely unknown. This is particularly the case for the sources of differences among families. Three types of processes can generate the variability among families: genetic, prenatal and postnatal. We first tested the family resemblance of dispersal behaviour in the common lizard (Lacerta vivipara). We then experimentally investigated the role of pre‐ and postnatal factors in the variability of dispersal among families. From 1989 to 1992, we studied dispersal of juveniles from pregnant females captured in the field and maintained in laboratory until parturition. We manipulated the conditions of gestation to test for prenatal effects on juvenile dispersal. We tested postnatal effects by releasing siblings of the same family in contrasted environments. We also examined covariances of natal dispersal with maternal and offspring traits. The results showed that: (1) dispersal behaviour was similar among siblings, (2) determinants of offspring dispersal differed between sexes and years, (3) offspring dispersal was related to litter sex‐ratio and offspring corpulence at birth, (4) postnatal conditions influenced male dispersal, (5) short‐term prenatal conditions (i.e. maternal conditions during gestation) influenced juvenile dispersal, varying per year, (6) long‐term prenatal conditions (i.e. maternal conditions during gestation in the previous year) could also influence juvenile dispersal (marginally significant). Thus, several types of processes determine natal dispersal in the common lizard. Resemblance among siblings can partly be explained by both pre‐ and postnatal effects. The environment seems to be the major factor influencing juvenile dispersal in this species, i.e. dispersal essentially appears condition‐dependent. The genetic basis of dispersal in vertebrates remains to be demonstrated by studies controlling for both prenatal and postnatal conditions.     

Stepping stones of life: natal dispersal in the group-living but noncooperative speckled warbler

In most cooperatively breeding birds the offspring of one sex, usually male, delays dispersal to remain on the natal territory and helps its parents to rear subsequent young. Thus delayed dispersal could be the first step in the evolution of cooperative breeding. We studied natal dispersal in a population of the group-living speckled warbler, Chthonicola sagittata, based on observations of a colour-banded population over 3 years. Unlike other group-living members of the Acanthizinae, all juvenile males in this population dispersed to settle on foreign territories as subordinates, which do not help rear the young. Speckled warblers showed all the life history traits that are thought to result in a saturated habitat and lead to delayed dispersal: they were sedentary, had high adult survival and had a male-biased sex ratio. However, they differed from other acanthizids in occurring at low density (0.18 birds/ha) on large breeding territories (6-12 ha), with a maximum of two males per territory. This may allow subordinates to live on foreign territories yet avoid aggression from dominants. A benefit of dispersal is that it provides an additional route to gaining a breeding vacancy. Dispersers can acquire vacancies on their new territory or on a neighbour's, but incest avoidance would be likely to constrain nondispersing males to neighbours' territories. A model of relative lifetime success showed that the survival benefits of natal philopatry are unlikely to outweigh this benefit of dispersal.     

Sex-bias and timing of natal dispersal in cooperatively breeding Puff-throated Bulbuls Alophoixus pallidus

While natal dispersal can have a significant impact on population dynamics, it is typically difficult to quantify. We investigated timing of natal dispersal of the cooperatively breeding Puff-throated Bulbul Alophoixus pallidus in a tropical evergreen forest by modelling the probability of staying in or dispersing from their natal territory whilst taking into account the effects of sex, group size, and the presence of helper(s). Birds did not disperse until the beginning of and during the breeding season following the hatching year. Dispersal was strongly female-biased both in frequency and distance: most females (95%) dispersed away from their natal territories, and of those relocated, traversed 2–7 territories. In contrast, 50% of males remained in the natal territory as helpers in their second year, while relocated dispersing males crossed 1–2 territories. Natal dispersal was not influenced by either group size or the presence of helpers. Males that fledged earlier in the breeding season exhibited higher rates of philopatry than the males that fledged later, but no correlation between fledging date and philopatry was observed in females. The probability of staying in the natal territory during the second year was 0.58 ± 0.14 SE and 0.05 ± 0.04 for males and females, respectively. These findings may add to our understanding of how natal dispersal can reflect social patterns and kin structure in cooperative breeding species from a little-studied tropical forest region.     

Increased lifetime reproductive success for Siberian jay (Perisoreus infaustus) males with delayed dispersal

In a crowded environment the natal territory could serve as a haven for young and inexperienced offspring until a breeding vacancy emerges. Delayed dispersal and association with kin could then offer adaptive benefits through an individual fitness gain. Here we report that delayed dispersal is associated with a higher lifetime individual fitness in Siberian jay (Perisoreus infaustus) males. Sons bred more successfully and had more reproductive events in life when they delayed dispersal. The higher lifetime reproductive success when sons disperse later in life is sufficient to promote postponement of natal dispersal, suggesting that dispersal is delayed due to ecological constraints on access to high-quality habitats. We argue that the maintenance of this variation in the timing of dispersal and reproductive success can be reconciled with non-genetic mechanisms driving dispersal. Social dominance within broods reflecting environmental conditions during growth is such a mechanism.     

Philopatry and natal dispersal of Montagu's harriers (Circus pygargus) breeding in Spain: a review of existing data

Natal dispersal is an important component of bird ecology, plays a key role in many ecological and evolutionary processes, and has important conservation implications. Nevertheless, detailed knowledge on natal dispersal is still lacking in many bird species, especially raptors. We review and compile existing information from five tagging programmes of juvenile Montagu's harriers (Circus pygargus) in different Spanish regions, with PVC rings or wing tags, to provide an assessment of philopatry and natal dispersal of the species in Spain. Only 7% of all tagged harriers were observed as breeders in subsequent years. The percentage of philopatric (i.e. breeding within 10?km of the natal site) males and females was lower that 5%. Overall, there were no sexual differences in percentage of philopatric birds or dispersal distances, but we found study area differences. The low philopatry observed suggests a high capacity for natal dispersal in this species, for both sexes, and therefore high genetic mixing between populations. Differences in philopatry between study areas may be influenced by the different observation effort or detectability, or else reflect different philopatric strategies among populations. Finally, we found no significant differences in philopatry rate or dispersal distances related to tagging method, suggesting that tagging technique has a smaller effect than monitoring effort or observation ease on observation probability. Developing tagging programmes at a small scale and without procuring very large-scale and intensive subsequent monitoring is not worthwhile for evaluating philopatry and natal dispersal in this species.     

Reverse sex-biased philopatry in a cooperative bird: genetic consequences and a social cause

The genetic structure of a group or population of organisms can profoundly influence the potential for inbreeding and, through this, can affect both dispersal strategies and mating systems. We used estimates of genetic relatedness as well as likelihood-based methods to reconstruct social group composition and examine sex biases in dispersal in a Costa Rican population of white-throated magpie-jays ( Calocitta formosa , Swainson 1827), one of the few birds suggested to have female-biased natal philopatry. We found that females within groups were more closely related than males, which is consistent with observational data indicating that males disperse upon maturity, whereas females tend to remain in their natal territories and act as helpers. In addition, males were generally unrelated to one another within groups, suggesting that males do not disperse with or towards relatives. Finally, within social groups, female helpers were less related to male than female breeders, suggesting greater male turnover within groups. This last result indicates that within the natal group, female offspring have more opportunities than males to mate with nonrelatives, which might help to explain the unusual pattern of female-biased philopatry and male-biased dispersal in this system. We suggest that the novel approach adopted here is likely to be particularly useful for short-term studies or those conducted on rare or difficult-to-observe species, as it allows one to establish general patterns of philopatry and genetic structure without the need for long-term monitoring of identifiable individuals.     

Habitat fragmentation shapes natal dispersal and sociality in an Afrotropical cooperative breeder

It remains poorly understood how effects of anthropogenic activity, such as large-scale habitat fragmentation, impact sociality in animals. In cooperatively breeding species, groups are mostly formed through delayed offspring dispersal, and habitat fragmentation can affect this process in two opposite directions. Increased habitat isolation may increase dispersal costs, promoting delayed dispersal. Alternatively, reduced patch size and quality may decrease benefits of philopatry, promoting dispersal. Here, we test both predictions in a cooperatively breeding bird (placid greenbul, Phyllastrephus placidus) from an Afrotropical cloud forest archipelago. Males born in fragmented forest dispersed about 1 year earlier than those born in continuous forest. Contrary to females, males also started to reproduce earlier and mostly settled within their natal patch. Females only rarely delayed their dispersal for more than 1 year, both in fragmented and continuous forests. Our results suggest that early male dispersal and reproduction is jointly driven by a decrease in the value of the natal territory and an increase in local breeding opportunities in fragmented forest. While plasticity in dispersal strategies of cooperative breeders in response to anthropogenic change is believed to optimize reproduction-survival trade-offs, to what extent it shapes the ability of species to respond to rapid environmental change remains to be studied.     

Benefits, constrainsts and the evolution of the family

Families form when offspring delay dispersal and remain associated with their parents into adulthood. What are the ultimate causes of such philopatry and prolonged association? Two schools of thought have emerged, providing seemingly opposing answers to this question - the 'benefits of philopatry' and the 'ecological constraints' schools. A recent threshold model for delayed dispersal helps clarify the confused semantics of these arguments and demonstrates the complimentarity of the two approaches. Many of the current advantages of family living may have evolved secondarily, however, suggesting that the initial origin of families occurred under conditions of severe competition for breeding vacancies.     

Family movements before independence influence natal dispersal in a territorial songbird

Dispersal behaviour in territorial species is typically assumed to be independent of parental behaviour except for the possible role of parental eviction from the natal territory. Great tits defend exclusive territories at the onset of breeding but after fledging undertake substantial excursions with dependent offspring, sometimes covering distances equivalent to ten or more breeding territories and even moving across open spaces into neighbouring woodlots. We show that postfledging family movements are significantly associated with subsequent dispersal directions of recruits by comparing observed angles of movement with a simulated distribution taking into account the patchy nature of the landscape. However, the extent of family movements did not predict dispersal distances. Our findings provide an explanation for previously observed similarities in dispersal direction between siblings in the same study population, as well as for effects of nest site location on dispersal. More generally we show the existence of a novel mechanism for parents to influence dispersal and fine-scale kinship structure among their offspring.     

Natal philopatry in passerine birds: genetic or ecological influences?

The degree of natal philopatry (the likelihood that individualsbreed at or near their place of origin) can influence the extentof inbreeding in animal populations. Passerine birds have beencited as typically showing high natal philopatry, and natalphilopatry has been proposed as an adaptation to promote optimalinbreeding. A review of published and unpublished studies ofpasserines showed that natal philopatry was typically low, somaintaining a high level of inbreeding appears relatively unimportantfor such birds. Rather, natal philopatry appeared to be morestrongly influenced by ecological factors. Migratory passerineexhibited low natal philopatry compared to resident passerines,as predicted if dispersal costs for young birds are an importantdeterminant of natal philopatry. The erroneous view that natalphilopatry for passerines is generally high has resulted froma reporting bias toward resident species that have sufficientnatal philopatry to study. Natal philopatry was found to beevolutionarily labile; populations of the same species and pairsof closely related species that differed in their degree ofisolation differed considerably in their degree of philopatry.Future studies of natal philopatry should consider both theecological factors that could affect dispersal costs and thereporting biases that influence which data on philopatry tendto be reported.     

Dispersal, migration, and offspring retention in saturated habitats

We examine the evolutionary stability of year-round residency in territorial populations, where breeding sites are a limiting resource. The model links individual life histories to the population-wide competition for territories and includes spatial variation in habitat quality as well as a potential parent-offspring conflict over territory ownership. The general form of the model makes it applicable to the evolution of dispersal, migration, partial migration, and delayed dispersal (offspring retention). We show that migration can be evolutionarily stable only if year-round residency in a given area would produce a sink population, where mortality exceeds reproduction. If this applies to a fraction of the breeding habitat only, partial migration is expected to evolve. In the context of delayed dispersal, habitat saturation has been argued to form an ecological constraint on independent breeding, which favors offspring retention and cooperative breeding. We show that habitat saturation must be considered as a dynamic outcome of birth, death, and dispersal rates in the population, rather than an externally determined constraint. Although delayed dispersal often associates with intense competition for territories, life-history traits have direct effects on stable dispersal strategies, which can often override the effect of habitat saturation. As an example, high survival of floaters selects against delayed dispersal, even though it increases the number of competitors for each breeding vacancy (the "habitat saturation factor"). High survival of territory owners, by contrast, generally favors natal philopatry. We also conclude that spatial variation in habitat quality only rarely selects for delayed dispersal. Within a population, however, offspring retention is more likely in high-quality territories.     

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

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

Genetic evidence for a family structure in stable social aggregations of the Australian lizard Egernia stokesii

In this study we used data from six unlinked microsatellite loci to examine stable aggregations of Egernia stokesii, from a population in the southern Flinders Ranges of South Australia. We show that these aggregations are comprised of breeding partners, their offspring from two or more cohorts, and related adults, providing the first genetic evidence of a family structure in any lizard species. Despite this high level of relatedness within aggregations, most breeding pairs were unrelated and partners were less closely related to each other than they were to other potential within-group partners. Where individuals dispersed, both sexes usually moved to social groups close to their natal group. Although both sexes showed natal philopatry, there was some evidence that females in groups were more related than males in groups. These data suggest that an active choice of unrelated partners and male-biased dispersal may be the mechanisms used by E. stokesii to avoid inbreeding within groups.