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.     

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.     

When it is costly to have a caring mother: food limitation erases the benefits of parental care in earwigs

The aggregation of parents with offspring is generally associated with different forms of care that improve offspring survival at potential costs to parents. Under poor environments, the limited amount of resources available can increase the level of competition among family members and consequently lead to adaptive changes in parental investment. However, it remains unclear as to what extent such changes modify offspring fitness, particularly when offspring can survive without parents such as in the European earwig, Forficula auricularia. Here, we show that under food restriction, earwig maternal presence decreased offspring survival until adulthood by 43 per cent. This effect was independent of sibling competition and was expressed after separation from the female, indicating lasting detrimental effects. The reduced benefits of maternal presence on offspring survival were not associated with higher investment in future reproduction, suggesting a condition-dependent effect of food restriction on mothers and local mother-offspring competition for food. Overall, these findings demonstrate for the first time a long-term negative effect of maternal presence on offspring survival in a species with maternal care, and highlight the importance of food availability in the early evolution of family life.     

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.     

Dispersal as a source of variation in age-specific reproductive strategies in a wild population of lizards

Dispersal syndromes describe the patterns of covariation of morphological, behavioural, and life-history traits associated with dispersal. Studying dispersal syndromes is critical to understanding the demographic and genetic consequences of movements. Among studies describing the association of life-history traits with dispersal, there is anecdotal evidence suggesting that dispersal syndromes can vary with age. Recent theory also suggests that dispersive and philopatric individuals might have different age-specific reproductive efforts. In a wild population of the common lizard (Zootoca vivipara), we investigated whether dispersive and philopatric individuals have different age-specific reproductive effort, survival, offspring body condition, and offspring sex ratio. Consistent with theoretical predictions, we found that young dispersive females have a higher reproductive effort than young philopatric females. Our results also suggest that the early high investment in reproduction of dispersive females trades-off with an earlier onset of senescence than in philopatric females. We further found that young dispersive females produce smaller offspring in lower body condition than do young philopatric females. Overall, our results provide empirical evidence that dispersive and philopatric individuals have different age-specific life-history traits.     

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.     

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.     

Reduced mortality selects for family cohesion in a social species

Delayed dispersal is the key to family formation in most kin-societies. Previous explanations for the evolution of families have focused on dispersal constraints. Recently, an alternative explanation was proposed, emphasizing the benefits gained through philopatry. Empirical data have confirmed that parents provide their philopatric offspring with preferential treatment through enhanced access to food and predator protection. Yet it remains unclear to what extent such benefits translate into fitness benefits such as reduced mortality, which ultimately can select for the evolution of families. Here, we demonstrate that philopatric Siberian jay (Perisoreus infaustus) offspring have an odds ratio of being killed by predators 62% lower than offspring that dispersed promptly after independence to join groups of unrelated individuals (20.6% versus 33.3% winter mortality). Predation was the sole cause of mortality, killing 20 out of 73 juveniles fitted with radio tags. The higher survival rate among philopatric offspring was associated with parents providing nepotistic predator protection that was withheld from unrelated group members. Natal philopatry usually involves the suppression of personal reproduction. However, a lower mortality of philopatric offspring can overcome this cost and may thus select for the formation of families and set the scene for cooperative kin-societies.     

The evolution of delayed dispersal in cooperative breeders.

Why do the young of cooperative breeders--species in which more than two individuals help raise offspring at a single nest--delay dispersal and live in groups? Answering this deceptively simple question involves examining the costs and benefits of three alternative strategies: (1) dispersal and attempting to breed, (2) dispersal and floating, and (3) delayed dispersal and helping. If, all other things being equal, the fitness of individuals that delay dispersal is greater than the fitness of individuals that disperse and breed on their own, intrinsic benefits are paramount to the current maintenance of delayed dispersal. Intrinsic benefits are directly due to living with others and may include enhanced foraging efficiency and reduced susceptibility to predation. However, if individuals that disperse and attempt to breed in high-quality habitat achieve the highest fitness, extrinsic constraints on the ability of offspring to obtain such high-quality breeding opportunities force offspring to either delay dispersal or float. The relevant constraint to independent reproduction has frequently been termed habitat saturation. This concept, of itself, fails to explain the evolution of delayed dispersal. Instead, we propose the delayed-dispersal threshold model as a guide for organizing and evaluating the ecological factors potentially responsible for this phenomenon. We identify five parameters critical to the probability of delayed dispersal: relative population density, the fitness differential between early dispersal/breeding and delayed dispersal, the observed or hypothetical fitness of floaters, the distribution of territory quality, and spatiotemporal environmental variability. A key conclusion from the model is that no one factor by itself causes delayed dispersal and cooperative breeding. However, a difference in the dispersal patterns between two closely related species or populations (or between individuals in the same population in different years) may be attributable to one or a small set of factors. Much remains to be done to pinpoint the relative importance of different ecological factors in promoting delayed dispersal. This is underscored by our current inability to explain satisfactorily several patterns including the relative significance of floating, geographic biases in the incidence of cooperative breeding, sexual asymmetries in delayed dispersal, the relationship between delayed dispersal leading to helping behavior and cooperative polygamy, and the rarity of the co-occurrence of helpers and floaters within the same population. Advances in this field remain to be made along several fronts.(ABSTRACT TRUNCATED AT 400 WORDS)     

Long-term consequences of early ontogeny in free-living Great Tits Parus major

Environmental factors during early development may have profound effects on subsequent life-history traits in many bird species. In wild birds, sex-specific effects of early ontogeny on natal dispersal and future reproduction are not well understood. The objective of this work was to determine whether hatching date and pre-fledging mass and condition of free-living Great Tits Parus major have any subsequent effect on individuals’ natal dispersal and reproductive performance at first breeding. Both males and females dispersed longer distances in coniferous than in deciduous forests, while dispersal was condition-dependent only in males (heavier as nestlings dispersed farther). In females, mass and condition at pre-fledging stage correlated significantly with clutch size, but not with subsequent reproductive performance as measured by fledging success or offspring quality. In contrast, heavier males as nestlings had higher future fledging success and heavier offspring in their broods compared with those in worse condition as nestlings. The hatching date of female as well as male parents was the only parental parameter related to the number of eggs hatched at first breeding. These results indicate that pre-fledging mass and condition predict subsequent fitness components in this bird species. We suggest that sex-specific relationships between a disperser’s condition and its selectivity with respect to breeding habitat and subsequent performance need to be considered in future models of life-history evolution.     

A theoretical model of the evolution of maternal effects under parent-offspring conflict

The evolution of maternal effects on offspring phenotype should depend on the extent of parent-offspring conflict and costs and constraints associated with maternal and offspring strategies. Here, we develop a model of maternal effects on offspring dispersal phenotype under parent-offspring conflict to evaluate such dependence. In the absence of evolutionary constraints and costs, offspring evolve dispersal rates from different patch types that reflect their own, rather than the maternal, optima. This result also holds true when offspring are unable to assess their own environment because the maternal phenotype provides an additional source of information. Consequently, maternal effects on offspring diapause, dispersal, and other traits that do not necessarily represent costly resource investment are more likely to maximize offspring than maternal fitness. However, when trait expression was costly, the evolutionarily stable dispersal rates tended to deviate from those under both maternal and offspring control. We use our results to (re)interpret some recent work on maternal effects and their adaptive value and provide suggestions for future work.     

Sex Allocation in California Oaks: Trade-Offs or Resource Tracking?

Trade-offs in sex resource allocation are commonly inferred from a negative correlation between male and female reproduction. We found that for three California oak species, aboveground annual net productivity (ANP) differences among individuals were primarily correlated with water availability and soil fertility. Reproductive biomass increased with ANP, but the relative allocation to reproduction was constant, indicating that reproduction tracked productivity, which in turn tracked site quality. Although there was a negative correlation between male and female reproduction, this was not the result of a resource investment trade-off, but rather a byproduct of the positive correlation between female reproductive biomass and ANP combined with the greater overall resource allocation to female, compared to male, function. Thus, we reject the hypothesis of a trade-off between these key life-history components within individuals of these species. For long-lived individuals, a plastic resource tracking response to environmental fluctuations may be more adaptive than directly linking life-history traits through trade-offs.     

The role of vegetative spread and seed dispersal for optimal life histories of clonal plants: a simulation study

Sexual and vegetative reproduction of clonal plants phenotypically differ in dispersal distance, in the phenology of offspring production and establishment, and in the success of establishment. We applied a combination of analytical and of spatially explicit individual-based simulation modelling to calculate long-term fitness. We predicted optimal clonal plant life histories in a parameter space spanned by stolon number, stolon internode length, and relative allocation to sexual and vegetative reproduction. For a given allocation to sexual reproduction and number of stolons, fitness was optimised for rather short internode lengths under small disturbances, and for the longest possible internodes under larger disturbances. A trade-off between length and number of vegetative spacers drew parameters away from their unrestricted optima. Now, intermediate length and number of spacers led to maximum fitness under large disturbances. Simultaneous trade-offs between sexual and vegetative reproduction and between the length and number of spacers could also lead to fitness optima at intermediate parameter values, depending on the success of seedling establishment. We demonstrated that spatial habitat structure (1) selects for an efficient use of available space either by optimum internode length or by investment into seeds, which disperse farther than vegetative spacers, and (2) leads to an interaction between trade-offs. We conclude, that dispersal distance, i.e. a spatial life-history component, and trade-offs must be included in considerations on adaptive evolution of clonal life histories.     

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.     

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.     

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.     

Sociality as a life-history tactic of ground squirrels

Summary Multi-variate analysis of life-history traits of 18 species of burrowing sciurids indicates that reproductive effort is determined by body-size energetics. Other traits, such as age adult weight reached, age of dispersal, length of time of gestation, were significantly correlated with body size. A principal component analysis suggested that the complex of life-history traits could be reduced to four components: body size (=weight), seasonality, specific reproductive effort, and maturity. The variation in the sociality index was best explained by age of first reproduction and age adult weight reached. Generally, species are more social when large body size combined with a relatively short growing season is associated with delayed dispersal and occurs in those species typically breeding for the first time at age two or older. Sociality in these species may have evolved through retention of daughters within the maternal home range as a means of continuing reproductive investment beyond weaning.     

Ecological constraints, life history traits and the evolution of cooperative breeding

The ecological constraints hypothesis is widely accepted as an explanation for the evolution of delayed dispersal in cooperatively breeding birds. Intraspecific studies offer the strongest support. Observational studies have demonstrated a positive association between the severity of ecological constraints and the prevalence of cooperation, and experimental studies in which constraints on independent breeding were relaxed resulted in helpers moving to adopt the vacant breeding opportunities. However, this hypothesis has proved less successful in explaining why cooperative breeding has evolved in some species or lineages but not in others. Comparative studies have failed to identify ecological factors that differ consistently between cooperative and noncooperative species. The life history hypothesis, which emphasizes the role of life history traits in the evolution of cooperative breeding, offers a solution to this difficulty. A recent analysis showed that low adult mortality and low dispersal predisposed certain lineages to show cooperative behaviour, given the right ecological conditions. This represents an important advance, not least by offering an explanation for the patchy phylogenetic distribution of cooperative breeding. We discuss the complementary nature of these two hypotheses and suggest that rather than regarding life history traits as predisposing and ecological factors as facilitating cooperation, they are more likely to act in concert. While acknowledging that different cooperative systems may be a consequence of different selective pressures, we suggest that to identify the key differences between cooperative and noncooperative species, a broad constraints hypothesis that incorporates ecological and life history traits in a single measure of 'turnover of breeding opportunities' may provide the most promising avenue for future comparative studies. Copyright 2000 The Association for the Study of Animal Behaviour.     

Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones

We know very little about physiological constraints on the evolution of life-history traits in general, and, in particular, about physiological and molecular adjustments that accompany the evolution of variation in lifespan. Identifying mechanisms that underlie adaptive variation in lifespan should provide insight into the evolution of trade-offs between lifespan and other life-history traits. Telomeres, the DNA caps at the ends of linear chromosomes, usually shorten as animals age, but whether telomere rate of change is associated with lifespan is unknown. We measured telomere length in erythrocytes from five bird species with markedly different lifespans. Species with shorter lifespans lost more telomeric repeats with age than species with longer lifespans. A similar correlation is seen in mammals. Furthermore, telomeres did not shorten with age in Leach's storm-petrels, an extremely long-lived bird, but actually lengthened. This novel finding suggests that regulation of telomere length is associated not only with cellular replicative lifespan, but also with organismal lifespan, and that very long-lived organisms have escaped entirely any telomeric constraint on cellular replicative lifespan.     

The effect of diet quality and wing morph on male and female reproductive investment in a nuptial feeding ground cricket

A common approach in the study of life-history trade-off evolution is to manipulate the nutrient content of diets during the life of an individual in order observe how the acquisition of resources influences the relationship between reproduction, lifespan and other life-history parameters such as dispersal. Here, we manipulate the quality of diet that replicate laboratory populations received as a thorough test of how diet quality influences the life-history trade-offs associated with reproductive investment in a nuptial feeding Australian ground cricket (Pteronemobius sp.). In this species, both males and females make significant contributions to the production of offspring, as males provide a nuptial gift by allowing females to chew on a modified tibial spur during copulation and feed directing on their haemolymph. Individuals also have two distinct wing morphs, a short-winged flightless morph and a long-winged morph that has the ability to disperse. By manipulating the quality of diet over seven generations, we found that the reproductive investment of males and females were affected differently by the diet quality treatment and wing morph of the individual. We discuss the broader implications of these findings including the differences in how males and females balance current and future reproductive effort in nuptial feeding insects, the changing nature of sexual selection when diets vary, and how the life-history trade-offs associated with the ability to disperse are expected to differ among populations.