Jan Komdeur

Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis).

We describe the development and initial application of a semiautomated parentage testing system in the Seychelles warbler (Acrocephalus sechellensis). This system used fluorescently labelled primers for 14 polymorphic microsatellite loci in two multiplex loading groups to genotype efficiently over 96% of the warbler population on Cousin island. When used in conjunction with the program cervus, this system provided sufficient power to assign maternity and paternity within the Seychelles warbler, despite the complications associated with its cooperative breeding system and a relatively low level of genetic variation. Parentage analyses showed that subordinate ‘helper’ females as well as the dominant ‘primary’ females laid eggs in communal nests, indicating that the Seychelles warbler has an intermediate level of female reproductive skew, in between the alternative extremes of helper‐at‐the‐nest and joint nesting systems. Forty‐four per cent of helpers bred successfully, accounting for 15% of all offspring. Forty per cent of young resulted from extra‐group paternity.

The evolution of mutual ornamentation

Many conspicuous ornamental traits in animals are expressed in both males and females. Despite this, most research has focused on sexually dimorphic ornamentation. Mutual ornamentation has often been viewed as a result of either a nonadaptive genetic correlation between the sexes or similar selection pressures in both sexes. Here, we review the theoretical underpinning and empirical evidence for these ideas. Few studies have attempted to test empirically whether a genetic correlation between the sexes can constrain the evolution of sexual dimorphism, and the results have been mixed. By contrast, there is good evidence that mutual ornaments can have a signal function in both sexes, especially in terms of mate choice. Other possible signalling functions have received little attention. Social status signalling is especially likely to be important, because competition over nonsexual resources is more balanced between the sexes than sexual competition. There is a need for experimental studies that explicitly test these hypotheses simultaneously in both sexes.

Experimental evidence for helping and hindering by previous offspring in the cooperative-breeding Seychelles warbler Acrocephalus sechellensis

Prebreeding Seychelles warblers (Acrocephalus sechellensis) frequently act as helpers on their natal territory, aiding in territory defence, predator mobbing, nestbuilding, incubation (only females) and feeding dependent young of their parents. In some cases helpers could attain breeding status (e.g. by joint-nesting) in their natal group and become co-breeders. Comparisons of group size and reproductive success on a given quality territory suggest that the presence of alloparents (helpers and cobreeders) significantly affects the reproductive success of their parents. The influence of alloparents on reproductive success was examined by removing alloparents from breeding units and comparing the success of natural-sized and artificially reduced groups. Removal experiments, controlled for territory quality, group size and breeder age, showed that the presence of one alloparent significantly improved the reproductive success of its parents. Analysis strongly suggests that this was entirely due to helping behaviour (i.e. providing care to offspring of their parents), thereby improving the helpers inclusive fitness benefits from staying at home. However, these experiments showed also that the presence of two or more alloparents in medium-quality territories significantly decreased reproductive success, compared with groups with one alloparent. Several lines of evidence suggest that this may have been due to the joint-nesting and reproductive competition that could occur in breeding groups, or simply to resource depression when a large number of previous offspring remained on their natal territory.

Is male care compromised by additional mating opportunity

In many animals, males contribute substantially to caring for their young but also have the opportunity to enhance their reproductive success by attracting additional mates or by seeking copulations with females that are already paired to other males. Sometimes, the opportunity to gain these additional matings coincides with periods when males are providing parental care. At such times, males might be expected to allocate time and effort to these alternative behaviours in a way that maximizes their overall reproductive success. But do they? Here, we examine the recent evidence for a tradeoff between parental effort and additional mating effort and highlight some of the factors that might influence how this conflict is resolved. We conclude that, in spite of the paucity of comprehensive studies, this tradeoff has a potentially important and often overlooked influence on parental behaviour in a range of taxa.

MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler

The existence and nature of indirect genetic benefits to mate choice remain contentious. Major histocompatibility complex (MHC) genes, which play a vital role in determining pathogen resistance in vertebrates, may be the link between mate choice and the genetic inheritance of vigour in offspring. Studies have shown that MHC-dependent mate choice can occur in mammal and fish species, but little work has focused on the role of the MHC in birds. We tested for MHC-dependent mating patterns in the Seychelles warbler (Acrocephalus sechellensis). There was no influence of MHC class I exon 3 variation on the choice of social mate. However, females were more likely to obtain extra-pair paternity (EPP) when their social mate had low MHC diversity, and the MHC diversity of the extra-pair male was significantly higher than that of the cuckolded male. There was no evidence that females were mating disassortatively, or that they preferred males with an intermediate number of MHC bands. Overall, the results are consistent with the ‘good genes’ rather than the ‘genetic compatibility’ hypothesis. As female choice will result in offspring of higher MHC diversity, MHC-dependent EPP may provide indirect benefits in the Seychelles warbler if survival is positively linked to MHC diversity.

Low-frequency songs lose their potency in noisy urban conditions

Many animal species communicate with their mates through acoustic signals, but this communication seems to become a struggle in urbanized areas because of increasing anthropogenic noise levels. Several bird species have been reported to increase song frequency by which they reduce the masking impact of spectrally overlapping noise. However, it remains unclear whether such behavioral flexibility provides a sufficient solution to noisy urban conditions or whether there are hidden costs. Species may rely on low frequencies to attract and impress females, and the use of high frequencies may, therefore, come at the cost of reduced attractiveness. We studied the potential tradeoff between signal strength and signal detection in a successful urban bird species, the great tit (Parus major). We show that the use of low-frequency songs by males is related to female fertility as well as sexual fidelity. We experimentally show that urban noise conditions impair male–female communication and that signal efficiency depends on song frequency in the presence of noise. Our data reveal a response advantage for high-frequency songs during sexual signaling in noisy conditions, whereas low-frequency songs are likely to be preferred. These data are critical for our understanding of the impact of anthropogenic noise on wild-ranging birds, because they provide evidence for low-frequency songs being linked to reproductive success and to be affected by noise-dependent signal efficiency.

DIRECT BENEFITS AND THE EVOLUTION OF FEMALE-BIASED COOPERATIVE BREEDING IN SEYCHELLES WARBLERS

Abstract.— Inclusive fitness benefits have been suggested to be a major selective force behind the evolution of cooperative breeding. We investigated the fitness benefits selecting for cooperative breeding in the Seychelles warbler, Acrocephalus sechellensis. A microsatellite‐based genotyping method was used to determine the relatedness of subordinates to group offspring in an isolated population of Seychelles warblers. The indirect and direct breeding benefits accruing to individual subordinates were then calculated for every successful breeding event over a three‐year period. We show that female subordinates frequently gained parentage and that this, combined with high levels of extra group paternity, resulted in low levels of relatedness between subordinates and non descendent offspring within a territory. Direct breeding benefits were found to be significantly higher than indirect kin benefits for both female and male subordinates. As predicted, female subordinates gained significantly more direct breeding opportunities and therefore higher inclusive fitness benefits by being a subordinate within a group than did males. This may explain why most subordinates in the Seychelles warbler are female.

The effect of kinship on helping in the cooperative breeding Seychelles warbler (Acrocephalus sechellensis)

It has previously been argued that the feeding of nestlings by non-parental birds may simply be an unselected consequence of delayed dispersal in cooperative breeding birds in which individuals follow simple rules such as ‘feed any begging mouth in my natal territory’. However, in the cooperative breeding Seychelles warblers (Acrocephalus sechellensis), helpers are more likely to help feed full siblings (both parents still alive) than half-siblings (one parent died), and do not help at all when the young are unrelated (both parents replaced). Helpers, helping both full siblings and half-siblings reduced their helping effort (food provisioning and period of helping) significantly when rearing young of lesser relatedness. These behaviours suggest that helping has been selected for in the context of promoting an individual’s indirect fitness, and that it is not simply a by-product of ‘provisioning behaviour’. The mechanism by which kin discrimination in helping is achieved appears to be associative learning; birds more often became helpers at nests belonging to related individuals who fed them (as a parent or a helper) when they were nestlings than at nests of related breeders who had not fed them in the nest.

Telomere length and dynamics predict mortality in a wild longitudinal study

Explaining variation in life expectancy between individuals of the same age is fundamental to our understanding of population ecology and life history evolution. Variation in the length and rate of loss of the protective telomere chromosome caps has been linked to cellular lifespan. Yet, the extent to which telomere length and dynamics predict organismal lifespan in nature is still contentious. Using longitudinal samples taken from a closed population of Acrocephalus sechellensis (Seychelles warblers) studied for over 20 years, we describe the first study into life‐long adult telomere dynamics (1–17 years) and their relationship to mortality under natural conditions (n = 204 individuals). We show that telomeres shorten with increasing age and body mass, and that shorter telomeres and greater rates of telomere shortening predicted future mortality. Our results provide the first clear and unambiguous evidence of a relationship between telomere length and mortality in the wild, and substantiate the prediction that telomere length and shortening rate can act as an indicator of biological age further to chronological age when exploring life history questions in natural conditions.

Pre-ovulation control of hatchling sex ratio in the Seychelles warbler

Females of some bird species have a high degree of control over the sex ratio of their offspring at laying. Although several mechanisms have been put forward to explain how females might control the sex of their eggs, virtually nothing is known. As females are the heterogametic sex in birds, adjustment of the clutch sex ratio could arise either by pre– or post-ovulation control mechanisms. The Seychelles warbler (Acrocephalus sechellensis) exhibits extreme adaptive egg sex ratio bias. Typically, warblers produce only single–egg clutches, but by translocating pairs to vacant habitat of very high quality, most females were induced to produce two–egg clutches. Overall, females skewed clutch sex ratios strongly towards daughters (86.6%). This bias was evident in the first egg, but critically, also in the second eggs laid a day apart, even when all absent, unhatched, or unsexed second eggs were assumed to be male. Although a bias in the first egg may arise through either pre– or post–ovulation mechanisms, the skew observed in second eggs could only arise through pre–ovulation control. Post–ovulation adjustment may also contribute to skewed hatchling sex ratios, but as sex–biased release of gametes is likely to be a more efficient process of control, pre–ovulation mechanisms may be the sole means of adjustment in this species. High fitness differentials between sons and daughters, as apparent in the Seychelles warblers, may be necessary for primary sex ratio adjustment to evolve.