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.     

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.     

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.     

Dispersal costs set the scene for helping in an atypical avian cooperative breeder

The ecological constraints hypothesis is suggested to explain the evolution of cooperative breeding in birds. This hypothesis predicts that the scene for cooperative breeding is set when ecological factors constrain offspring from dispersal. This prediction was tested in the atypical cooperative breeding system of the long-tailed tit, Aegithalos caudatus, by comparing the degree of philopatry and cooperation in an isolated and a contiguous site whilst experimentally controlling for confounding aspects of reproduction. No difference was found between the two sites in the survival of offspring but a greater proportion were found to remain philopatric in the isolated site. This difference was caused by greater philopatry of normally dispersive females suggesting, as predicted, that dispersal costs were greater from this site. Furthermore, a greater proportion of males and females cooperated following breeding failure in the isolated site than in the contiguous site. Thus, as has been suggested for typical avian cooperative breeders, dispersal costs, relative to philopatric benefits, appear to set the scene for cooperative breeding in long-tailed tits.     

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.     

The evolution of cooperative breeding in birds: kinship,dispersal and life history

The evolution of cooperation among animals has posed a major problem for evolutionary biologists, and despite decades of research into avian cooperative breeding systems, many questions about the evolution of their societies remain unresolved. A review of the kin structure of avian societies shows that a large majority live in kin-based groups. This is consistent with the proposed evolutionary routes to cooperative breeding via delayed dispersal leading to family formation, or limited dispersal leading to kin neighbourhoods. Hypotheses proposed to explain the evolution of cooperative breeding systems have focused on the role of population viscosity, induced by ecological/demographic constraints or benefits of philopatry, in generating this kin structure. However, comparative analyses have failed to generate robust predictions about the nature of those constraints, nor differentiated between the viscosity of social and non-social populations, except at a coarse level. I consider deficiencies in our understanding of how avian dispersal strategies differ between social and non-social species, and suggest that research has focused too narrowly on population viscosity and that a broader perspective that encompasses life history and demographic processes may provide fresh insights into the evolution of avian societies.     

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.     

Extended parental care and delayed dispersal: northern, tropical, and southern passerines compared

Using modern comparative methods, we found that both time toindependence and time with parents were significantly longerin southern hemisphere and tropical birds than in northern hemisphereones. These differences held even after removing Australianpasserines or cooperatively breeding species, and they do notdepend on habitat, diet, or migration pattern. In southern hemisphereand tropical regions, both cooperative breeding and non-cooperativeparents continue to feed their young for a similar length oftime, but cooperative breeders allow them to stay longer intheir natal territory after they become nutritionally independent.Nevertheless, the young of non-cooperative species stay longerwith their parents than do the young of non-cooperative speciesin the temperate northern hemisphere. The fact that extendedperiods of post-fledging parental care are widespread amongpasserines provides further empirical support for the view thatlife histories of southern and tropical birds are ‘slow,’with small clutches, extended parental care, and long lifespan;parents take care of fewer young for longer. These results supportrecent theoretical models that predict that high adult survivaland low turnover of territory owners generally favor natal philopatry.We suggest that the reasons why some species (with or withoutcooperative breeding) exhibit natal philopatry and others donot lie in the balance between productivity and survival ofadults and of retained or dispersing offspring.     

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.     

Dispersal strategies in Tasmanian native hens (Gallinula mortierii)

Individuals in cooperatively breeding species face a complexset of decisions when they reach reproductive maturity. Duringan 8-year study, we examined the histories of 214 Tasmaniannative hens (Gallinula mortierii) from hatching to examinethe strategies they used to acquire breeding positions andthe reproductive success they experienced in those breedingpositions. Two-thirds of young delayed dispersal from theirnatal groups for at least a year. Ecological constraints werea partial cause of delayed dispersal; high-quality territorieswere rare and remained occupied due to high adult survivorship.There were also clear benefits of philopatry. Individuals thatinherited breeding positions on their natal territories gainedbetter quality positions and experienced higher reproductivesuccess in their first breeding attempts than did individualswho dispersed to other groups. Multivariate analyses showedthat the method of acquisition of breeding positions was theonly factor significantly related to the quality of the breedingpositions attained. Males were more likely to inherit breeding positions in their natal groups than were females. The compositionsof individuals' natal groups had no effect on whether theyinherited breeding positions or dispersed. In contrast, thecompositions of groups did appear to affect whether other birdsdispersed into them, with birds rarely moving into groups thatcontained breeders or nonbreeders of the same sex as the potential dispersers. Short-term removals of breeders confirmed this finding.These results suggest that both ecological constraints andbenefits of philopatry explain delayed dispersal in this species.     

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.     

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.     

Family living among birds

Family cohesion in birds is often explained as a product of limitations on breeding opportunities leading to delayed dispersal among the offspring. Yet, it is not independent reproduction but floating (queuing outside the natal territory for a breeding opportunity) that is the alternative to delaying dispersal. In contrast to a strong phylogenetic bias in cooperative breeding that has been taken to indicate a hard-wired behaviour maintained by evolutionary inertia, offspring behaviour is plastic and facultative in group living in the short term, indicating that family cohesion is under selection. Non-breeding offspring could gain inclusive fitness that would promote family cohesion from delaying dispersal and providing alloparental care to subsequent broods to boost group productivity. This holds in particular for offspring hatched from early broods in multi-brooded species that have the opportunity to gain inclusive fitness from help in rearing siblings hatched from later broods in the same season. Yet, seasonality will circumscribe the potential for alloparenting to be the immediate factor selecting for family cohesion. The option of gaining inclusive fitness from providing alloparental care is not open to the offspring among single-brooded species until after they have survived a non-breeding season, rather indicating kin cooperation returning enhanced survival prospects from general group living effects as a more immediate factor selecting for family cohesion. Indeed, a variety of family groups maintained in the absence of alloparental care underlines the capacity of general group living enhancing survival as a primary agent selecting for family cohesion. These seasonal constraints on fitness components selecting for family cohesion may contribute to the large scale geographical pattern with a relative paucity of family cohesions among bird species in the northern hemisphere.     

Sex biased natal dispersal in a closed, saturated population of Seychelles warblers Acrocephalus sechellensis

The distances that individuals disperse, from their natal site to the site of first breeding and between breeding sites, have important consequences for the dynamics and genetic structure of a population. Nearly all previous studies on dispersal have the problem that, because the study area encompassed only a part of the population, emigration may have been confounded with mortality. As a result long-distance dispersers may have been overlooked and dispersal data biased towards short distances. By studying a virtually closed population of Seychelles warblers Acrocephalus sechellensis we obtained almost unbiased results on several aspects of dispersal. As in the majority of other avian species, natal dispersal distance was female biased in the Seychelles warbler. Female offspring also forayed further from the natal territory in search of breeding vacancies than male offspring. The sex bias in natal dispersal distance did, however, depend on local breeding density. In males, dispersal distance decreased as the number of territories bordering the natal territory increased, while in females, dispersal distance did not vary with local density. Dispersal by breeders was rare and, unlike in most species, distances did not differ between the sexes. We argue that our results favour the idea that the sex bias in natal dispersal distance in the Seychelles warbler is due to inbreeding avoidance and not resource competition or intrasexual competition for mates.     

Avian cooperative breeding: Old hypotheses and new directions

In cooperatively breeding birds, individuals that appear capable of reproducing on their own may instead assist others with their breeding efforts. Research into avian cooperative breeding has attempted to reconcile the apparent altruism of this behaviour with maximization of inclusive fitness. Most explanations of cooperative breeding have suggested that philopatry is enforced by ecological constraints, such as a shortage of resources critical to breeding. Non-dispersers may then benefit both directly and indirectly from contributing at the nest. Recent research has shown that such benefits may be sufficient to promote philopatry, without the need for ecological constraints, and emphasizes that consideration of both costs and benefits of philopatry is essential for a comprehensive approach to the problem. The growing body of data from long-term studies of different species should combine with an improved phylogenetic perspective on cooperative breeding, to provide a useful base for future comparative analyses and experimentation.     

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.     

Fighting to stay: the role of sibling rivalry for delayed dispersal

In many bird species with delayed dispersal, siblings differ in how long they postpone independence. Some offspring remain with their parents for a year or more and generally forego personal reproduction, while other siblings disperse in the first summer of life. We studied the basis for this variation by following dispersal among newly fledged Siberian jays, Perisoreus infaustus, carrying radiotransmitters. Postponed dispersal was the preferred option. Sibling rivalry preceded dispersal, and the larger and socially dominant siblings within broods were more likely to stay. No sex effect was found: males and females were just as likely to delay dispersal. This role of sibling rivalry shows that models explaining delayed dispersal based on ecological constraints outside the natal territory are too simplistic. The process of within-brood competition in determining which individuals disperse and which ones delay dispersal indicates that there are benefits to be gained from remaining in the natal territory. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Ecological constraints and benefits of philopatry promote group-living in a social but non-cooperatively breeding fish

Why non-breeding subordinates of many animal societies tolerate group-living remains a pertinent question in evolutionary biology. The ecological constraints and benefits of philopatry hypotheses have the potential to explain the maintenance of group-living by specifying the ecological conditions favouring delayed dispersal over independent breeding by subordinates. In this study, I used field and laboratory experiments to investigate the role of ecological and social factors on the dispersal decisions of non-breeding subordinates in the coral-dwelling fish, Paragobiodon xanthosomus (Gobiidae). Subordinate dispersal was strongly influenced by ecological constraints (habitat saturation and risks of movement) and benefits of philopatry (relative coral size). Social factors, namely social rank and forcible eviction, did not affect the occurrence of subordinate dispersal. These results suggest that selection has favoured subordinate P. xanthosomus, which employ a mixed strategy—switching tactics in response to three ecological factors—despite having low mobility and extreme habitat-specific requirements. Furthermore, this study demonstrates the generality of the ecological constraints and benefits of philopatry hypotheses as explanations for group-living in species where subordinates are unrelated to breeders, provide no help and do not strictly delay dispersal.     

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.     

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.