Female-biased Natal Dispersal Research Articles

Lone male loser? Effects of spatial isolation on male pairing success in the Ortolan Bunting (Emberiza hortulana)

Cover photo: Male Ortolan Bunting. Photo: Frode Falkenberg. In small, isolated or fragmented bird populations, past studies have shown that there can be a high proportion of unpaired males. Low male pairing success is suggested to be the result of female-biased natal dispersal and low female recruitment. Indirect evidence indicates that such an effect operates among populations with different degrees of isolation, but little is known of how isolation affects male pairing success within populations. The Norwegian population of Ortolan Buntings (Emberiza hortulana) is distributed in about 50 discrete patches in an area of nearly 500 km2. In this study, we examined whether patch isolation and individual male isolation affected male pairing success. The population has a strongly male-biased sex ratio, with almost half of all males being unpaired. We found that male pairing successs was negatively related to isolation of patches and isolation of individual males in most analyses, and with significant effects in particular in some analyses of individual isolation. Patch population size was measured as the total number of males observed in a particular patch in a specific year and did not have an effect on male pairing success, and was not related to patch isolation. Even though some tests were statistically significant, the magnitude of effects were small and there was large variance in male pairing success. Variance in success suggests that other factors than isolation such as male age or experience may be just as important for male fitness within our study population. Furthermore, we suggest that small effects of isolation were due to the ability of Ortolan Buntings to move large distances within the breeding season, and that isolation effects on small spatial scales are more likely for species with restricted dispersal, such as resident species or species with high population density.

Genetic structure confirms female-biased natal dispersal in the White-tailed Eagle population of the Carpathian Basin

Genetic structure confirms female-biased natal dispersal in the White-tailed Eagle population of the Carpathian Basin

Inbreeding and inbreeding avoidance in wild giant pandas

Inbreeding can have negative consequences on population and individual fitness, which could be counteracted by inbreeding avoidance mechanisms. However, the inbreeding risk and inbreeding avoidance mechanisms in endangered species are less studied. The giant panda, a solitary and threatened species, lives in many small populations and suffers from habitat fragmentation, which may aggravate the risk of inbreeding. Here, we performed long-term observations of reproductive behaviour, sampling of mother-cub pairs and large-scale genetic analyses on wild giant pandas. Moderate levels of inbreeding were found in 21.1% of mating pairs, 9.1% of parent pairs and 7.7% of panda cubs, but no high-level inbreeding occurred. More significant levels of inbreeding may be avoided passively by female-biased natal dispersal rather than by breeding dispersal or active relatedness-based mate choice mechanisms. The level of inbreeding in giant pandas is greater than expected for a solitary mammal and thus warrants concern for potential inbreeding depression, particularly in small populations isolated by continuing habitat fragmentation, which will reduce female dispersal and increase the risk of inbreeding.

The Evolution of Male-Biased Dispersal under the Joint Selective Forces of Inbreeding Load and Demographic and Environmental Stochasticity.

Sex-biased natal dispersal is widespread, and its significance remains a central question in evolutionary biology. However, theory so far fails to predict some of the most common patterns found in nature. To address this, we present novel results from an individual-based model investigating the joint roles of inbreeding load, demographic stochasticity, environmental stochasticity, and dispersal costs for the evolution of sex-biased dispersal. Most strikingly, we found that male-biased natal dispersal evolved in polygynous systems as a result of the interplay between inbreeding avoidance and stochasticity, whereas previous theory, in contrast to empirical observations, predicted male philopatry and female-biased natal dispersal under inbreeding load alone. Furthermore, the direction of the bias varied according to the nature of stochasticity. Our results therefore provide a unification of previous theory, yielding a much better qualitative match with empirical observations of male-biased dispersal in mate defense mating systems.

Sex-specific mortality costs of dispersal during the post-settlement stage promote male philopatry in a resident passerine

The costs and benefits of dispersal that select for sex-biased dispersal are still poorly understood. Many studies examine fitness consequences of dispersal after first breeding, while dispersal costs are most likely paid before first breeding during the movement, settlement, and post-settlement stages. We studied survival correlates of dispersal between flock settlement and first breeding during the first winter of juvenile willow tits (Poecile montanus), a small passerine that has female-biased natal dispersal, but shows no dispersal-associated survival differences after first breeding. This resident food-hoarding species winters in small stable non-kin territorial flocks. We collected capture-recapture data by following flocks from autumn to the following spring. We compared monthly survival and return rates of juveniles that were born and recruited within the study area (philopatric juveniles) and juveniles that originated from outside the study area (immigrant juveniles). Among males, survival was highest for philopatric juveniles whereas survival of females was higher among immigrant juveniles, providing one explanation for the female-biased natal dispersal observed in the species. Philopatric males may benefit from prior residency either through increased site familiarity and knowledge of winter food resources and/or by gaining higher social ranks during flock establishment. However, rank data provided little support for the latter hypothesis. Other mechanisms such as increased ability to find high-quality flocks and mates may be important for female survival. Our results provide further evidence that dispersal costs are paid mainly before first breeding and that sex-specific costs of dispersal play a role in the evolution of sex-biased dispersal. This paper shows that female-biased dispersal can be a consequence of sex-specific costs and benefits of dispersal during the post-settlement stage of the dispersal process which is a very poorly understood stage in dispersal theory. By examining correlates of dispersal before rather than after first breeding as it is usually done, our study aids in understanding the selection pressures modifying dispersal strategies. Our results have wide applicability because there are many resident taxa similar to the willow tit (our study species) that have a settlement stage and a prolonged non-reproductive phase before their first reproduction.

Intersexual difference in early natal dispersal: abrupt departure by females and gradual emigration by males in Tengmalm’s Owl Aegolius funereus

The decision to emigrate from the natal area can influence future fitness prospects, yet detailed data on sex-specific juvenile dispersal behaviour is still lacking for most bird species. We tracked 13 radio-tagged Tengmalm’s Owl Aegolius funereus juveniles from 13 different nests from fledging to independence and onwards. Six out of the seven female juveniles departed abruptly and disappeared from the natal area. In contrast, only one male juvenile departed abruptly, whereas the other five males and one female remained in the study area until tracking was terminated. We propose two alternative interpretations: (1) females initiated natal dispersal earlier than males, or (2) the manner of dispersal differed between the sexes, with females departing abruptly, and males moving gradually out of the natal area. We found no statistically significant influence of body condition or date of independence on dispersal behaviour. We suggest that early onset of dispersal and fast movements out of the natal area may increase a juvenile female’s chances of successful breeding in the following spring. In contrast to females, male Tengmalm’s Owls rarely breed as 1-year-olds, and the benefits of early/abrupt dispersal may be lower for juvenile males. We suggest that female-biased natal dispersal in Tengmalm’s Owl may come about through relatively higher lifetime reproductive success of early dispersing in females than in males.

Learned vocal group signatures in the polygynous bat Saccopteryx bilineata

Vocal group signatures facilitate group cohesion or the exclusion of nongroup members and thus greatly affect the social system of any given species. This is especially significant for highly mobile animals such as bats. The greater sac-winged bat, Saccopteryx bilineata, lives in a harem-based resource defence polygyny with patrilineal kin groups and female-biased natal dispersal. Pups of both sexes produce isolation calls to elicit maternal care. We analysed isolation calls from 25 pups born in seven different social groups in search of vocal signatures. In addition to a constant individual signature, isolation calls exhibited a group signature that became more prominent during ontogeny. Call convergence of fellow pups was independent of relatedness among pups and not driven by maturation effects, showing that the group signature was acquired through social modification, a form of vocal production learning. Behavioural observations of free-living bats indicated that isolation calls were used by adult males to appease more dominant males and to court unfamiliar females. The learned group signature in isolation calls may function as a ‘password’ that reliably associates individuals with their natal colony. This, in turn, could facilitate male harem acquisition and female inbreeding avoidance in the polygynous S. bilineata. The flexibility inherent in the vocal-learning process guarantees that crucial information can be promoted even under shifting social circumstances.

Sex-specific fitness consequences of dispersal in Siberian jays

In most birds, natal dispersal is female-biased, but the selective pressures leading to this pattern have rarely been explored with comprehensive data on lifetime reproductive success. In territorial birds, the benefit of philopatry should be higher for males than for females when males establish territories for which knowledge about the local environment is important. As females may use male characteristics for mate choice, and hence indirectly for territory choice, the benefit from the direct knowledge of the local environment may be lower for females than males. We tested this hypothesis using data from a long-term study of group living corvids, the Siberian jays (Perisoreus infaustus). In this species, the socially dominant offspring delay dispersal while the sub-dominant offspring leave the family group directly after reaching independence. Our results show that natal dispersal distance (a proxy for local knowledge) was related to sex and dispersal timing (a proxy for “quality”): Females and early dispersers traveled further on average than males and delayed dispersers. Furthermore, dispersal distance and timing were negatively related to the number of recruits produced over an individual’s lifetime in males, but not in females. Hence, the results support the hypothesis that the female-biased natal dispersal found in this and other bird species may come about through higher lifetime reproductive success of philopatric males than females.

Female-biased natal dispersal in the Siberian flying squirrel

Natal dispersal is usually sex biased in birds and mammals. Female-biased natal dispersal is the prevailing pattern in birds but is rare among mammals. Hypotheses explaining sex bias in dispersal include the mate-defense mating hypothesis, which predicts male-biased dispersal, the resource-defense hypothesis predicting female-biased dispersal, and the competition hypothesis, which predicts that if dispersal is caused by competition for resources between sexes, then the subdominant sex will disperse. We studied natal dispersal of Siberian flying squirrels Pteromys volans using radio telemetry in Southern Finland in 1996-2004. Of 86 juveniles that survived over the dispersal period, almost all young females dispersed from the natal site, whereas almost 40% of males were philopatric. Dispersal was farther for females than males. Females began dispersal on average 2 weeks earlier than males and were lighter in mass at the onset of dispersal than later dispersing males. No mate- or resource-defense mating system could be found among males, but females seemed to defend nest and apparently food resources, in contrast to the expectation of dispersal bias in resource-defense systems. Competition for resources between sexes does not explain female bias either: in the flying squirrel, the female seems to be the dominant sex. We propose that young females are subordinate to their mothers and have to disperse to find a vacant, suitable site for reproduction.

Natal dispersal patterns are not associated with inbreeding avoidance in the Seychelles warbler

In this study, we test whether patterns of territory inheritance, social mate choice and female-biased natal dispersal act as inbreeding avoidance mechanisms in the cooperatively breeding Seychelles warbler. Our results show that Seychelles warblers do not reduce the likelihood of inbreeding by avoiding related individuals as mates. The occurrence of natural and experimentally induced territory inheritance did not depend on whether the remaining breeder was a parent of the potential inheritor or an unrelated breeder. Furthermore, dispersing individuals were no less related to their eventual mates than expected given the pool of candidates they could mate with. The female bias in natal dispersal distance observed in the Seychelles warbler does not facilitate inbreeding avoidance because, contrary to our prediction, there was no sex difference in the clustering of related opposite sex breeders around the natal territories of dispersers. As a result, the chance of females mating with relatives was not reduced by their greater dispersal distance compared with that of males.

Viability of an endangered population of ortolan buntings: The effect of a skewed operational sex ratio

Population viability analyses (PVAs) are based on basic demographic parameters such as breeding success, juvenile and adult survival. However, no PVAs have included the operational sex ratio (OSR). The Norwegian population of ortolan buntings ( Emberiza hortulana) is characterized by a strongly skewed OSR (almost half of all males are unpaired). We assessed the effect of a skewed OSR on annual growth rate ( λ). Based on empirical data the deterministic growth rate was negative ( λ = 0.82), and mean time to extinction was 21.8 years. Model parameters had to be increased substantially compared to the empirical mean values to achieve λ = 1.0 (clutch size from 4.25 to 8.06, juvenile survival from 17.6% to 33.5%, adult survival from 62.9% to 80.8%, and proportion of males breeding from 52.4% to 99.8%). Using low, mean and high empirical parameter estimates, we examined 36 scenarios for population development. Only five resulted in values exceeding λ = 1.0, of which four required an OSR of 1:1. Correlations between inter-annual population change and demographic parameters indicated that the proportion of males breeding matched the observed population trend best. Because breeding success, juvenile and adult survival were within the normal range seen among other bird species of similar body size, we suggest that the skewed OSR is the major factor limiting population growth. Skewed OSRs may be particularly common in small and isolated bird populations, because of female-biased natal dispersal, and should therefore be considered in all PVAs of endangered bird species.

Asymmetrical incest avoidance in the choice of social and genetic mates

Mating with close relatives generally results in reduced reproductive success (inbreeding depression) because it increases the risk that rare deleterious recessive alleles will be expressed in offspring. None the less, incest may occur when animals have incomplete knowledge about relatedness or when the costs of avoiding inbreeding are high. Over a 17-year period, Savannah sparrows, Passerculus sandwichensis ,i n an island population rarely paired incestuously (9 of 1110 pairs, 15 of 1609 nesting attempts). All but one case of close inbreeding (coefficient of inbreeding, F � 0.25) involved 1-year-old males breeding for the first time, whereas more than half of the cases involved females that were 3 years old or older. Father–daughter matings were avoided completely. Incest avoidance was apparent in the choice of genetic as well as social mates. Paternity analysis using microsatellites revealed that birds nearly always refrained from choosing close relatives as genetic mates. These results support a model of asymmetrical incest avoidance, which predicts differences in the likelihood of incestuous matings as a function of sex, age and relationship, even when coefficients of inbreeding are identical. The model and results also emphasize the importance of distinguishing types of inbreeding and considering the social and historical context of animals’ mating choices. The model may help to explain such patterns as female-biased natal dispersal in birds.

Natal Dispersal in Florida Sandhill Cranes

Knowledge of natal dispersal is essential for understanding how nonmigratory crane populations expand and how this process can be augmented by relocation or reintroduction. We conducted a study from 1988 to 1999 and found that natal dispersal in Florida sandhill cranes (Grus canadensis pratensis) was female-biased. Females (n = 16) dispersed an average of 11.6 km from their natal territory. Male (n = 12) dispersal averaged 3.9 km. This difference was significant (P 0.05) or affected by gender (P > 0.05). Male philopatry and female-biased natal dispersal are consistent with theories of a resource-based mating system. Timing of the start of dispersal (family breakup) was found to be more closely tied to the female's laying the subsequent clutch than to the age of the juvenile crane.

Female‐biased dispersal, low female recruitment, unpaired males, and the extinction of small and isolated bird populations

Small and isolated populations are usually assumed to be at a high risk of extinction due to environmental or demographic stochasticity, genetic problems, or too little immigration. In birds, natal dispersal is usually female‐biased, but the consequences of such a pattern on vulnerability to extinction of isolated populations has not received much attention before. In this paper I derive predictions as to how female‐biased natal dispersal may differentially affect the extinction risk of populations and species with contrasting distributions, migratory behaviours, life histories and mating systems. Female‐biased dispersal will lead to male‐biased sex ratios in small, isolated or fragmented populations, in particular because recent research has shown that females often have a limited ability to search for mates and may therefore effectively be lost from the breeding population if they disperse into areas empty of conspecifics. I reviewed published studies on birds and found that a high proportion of unpaired males is common in isolated populations or populations in small habitat fragments. Dispersal of females may therefore increase the vulnerability to extinction of small or isolated populations, or populations at the periphery of a species’ distribution range. I also predict that vulnerability to extinction should be greater for migratory than for resident species and greater for short‐lived than for long‐lived species because of differences in the time available for females to locate unpaired males. Further, extinction risk may also be greater for birds than for mammals due to differences in which sex disperses and patterns of parental care. Finally, mating system will also affect vulnerability to extinction when natal dispersal leads to biased sex ratios. I review available evidence for these predictions (e.g. songbird declines in North America) and discuss implications for conservation.