Raoul A. Mulder

Helpers liberate female fairy-wrens from constraints on extra-pair mate choice

In cooperatively breeding superb fairy-wrens (Malurus cyaneus), all males contribute to the feeding and defence of young. Despite the expectation that such paternal care should be directed only to relatives, DNA fingerprinting revealed that most offspring (76%, 138 out of 181) were sired by extra-group males that contributed no care, and that almost all broods (95%, 38 out of 40) contained young sired by extra-group fathers. This is the highest known incidence of cuckoldry. This remarkable mating system is produced by female control of fertilization and consistent preference for certain extra-group male genotypes. This choice leads to the production of sons that also gain extra-group fertilizations. One constraint on the extra-pair mate choice of females is the level of parental assistance received from males. Males living in pairs contribute relatively more parental care and are more likely to gain paternity in one of their broods (85%, 11 out of 13) than dominant males in multi-male cooperative groups (30%, 8 out of 27). In groups helpers compensate for the lower parental assistance of dominant males, so the total feeding rate is similar between pairs and groups. This suggests that females allow males in pairs more paternity to ensure their assistance with parental care. Helpers provide an alternative source of paternal investment, and allow females to express unrestricted mate choice. Mating options for females in other species with female control of fertilization may also reflect a trade-off between acquiring the genes of high-quality males for their offspring and parental care of those offspring.

Fairy-Wren Helpers often Care for Young to Which they are Unrelated

In contrast to most cooperatively breeding birds, helpers in groups of superb fairy-wrens (Malurus cyaneus) are often not related to the young they provision because frequently their m others either die or move, and because most fertilizations are gained by males which are outside the group that rear the young. All helpers provision broods, but this care does not enhance productivity when com pared to unassisted pairs. Helpers provide care regardless of the degree of relatedness to the young they provision. Therefore, it is unlikely that helping behaviour in fairy-wrens is maintained sim ply by indirect benefits gained through the production of non-descendant kin. Alternative explanations of care: ‘unselected’ hypothesis; enhanced future probability of breeding; and direct increases in reproductive success can also be rejected. Our data support the view that helping is a payment to breeders which allows helpers to stay in the group.

Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird

Recent studies of non–social animals have shown that sexually selected traits signal at least one measure of genetic quality: heterozygosity. To determine whether similar cues reveal group quality in more complex social systems, we examined the relationship between territory size, song structure and heterozygosity in the subdesert mesite (Monias benschi), a group–living bird endemic to Madagascar. Using nine polymorphic microsatellite loci, we found that heterozygosity predicted both the size of territories and the structure of songs used to defend them: more heterozygous groups had larger territories, and more heterozygous males used longer, lower–pitched trills in their songs. Heterozygosity was linked to territory size and song structure in males, but not in females, implying that these traits are sexually selected by female choice and/or male–male competition. To our knowledge, this study provides the first direct evidence in any animal that territory size is related to genetic diversity. We also found a positive association between seasonal reproductive success and heterozygosity, suggesting that this heritable characteristic is a reliable indicator of group quality and fitness. Given that heterozygosity predicts song structure in males, and can therefore be determined by listening to acoustic cues, we identify a mechanism by which social animals may assess rival groups, prospective partners and group mates, information of potential importance in guiding decisions related to conflict, breeding and dispersal.

Can we measure the benefits of help in cooperatively breeding birds: the case of superb fairy-wrens Malurus cyaneus ?

1. Correlational studies of reproductive success are plagued by difficulty over the direction of causation. For example, improved reproductive success with age can result from increased experience or reproductive effort, or selection against low-quality phenotypes that survive poorly. An association between supernumeraries and reproductive success in cooperative breeders can arise either because supernumeraries boost productivity, or productive territories accumulate supernumeraries. 2. Paired comparisons of parents sampled with and without supernumeraries have recently been widely applied to quantify help. However, Dickinson & Hatchwell (2004) have argued that this approach is flawed. They conjectured that those groups that gain supernumeraries are a biased superior sample of those that initially lack supernumeraries, while groups that lose supernumeraries will be a sample of inferior cooperative groups. They predict that these biased comparisons will underestimate the effect of help. 3. This conjecture has neither been explored theoretically, nor empirically tested. We use data from a 19-year study of the superb fairy-wren Malurus cyaneus to examine the conjecture and derive predictors of annual reproductive success in this species. 4. We introduce statistical models of reproductive success based on a zero-inflated Poisson link function to identify three strong correlates of reproductive success: high spring rainfall, progress from the first to later years of life, and acquisition of supernumeraries. 5. First year females that died after breeding and those that survived to breed again had similar productivity. As female productivity improves with age, increased reproductive skill or effort is implicated rather than selection against inferior phenotypes. 6. We argue that the Dickinson-Hatchwell conjecture does not constrain paired comparisons in M. cyaneus. The dominant male and breeding female gain no immediate fecundity advantage from supernumeraries. 7. Effects on the future survival of dominants are even more difficult, as while helpers could enhance survival of dominants, a territory that facilitates survival should also accumulate philopatric supernumeraries. Males, the philopatric sex, did not survive better on territories with supernumeraries. However, females, the dispersive sex, had higher survival as the number of supernumeraries increased, because helpers allowed them to reduce the costs of reproduction. These data exacerbate the paradox posed by previously reported costs that supernumeraries impose on dominant males.

Sperm competition and the reproductive anatomy of male superb fairy-wrens

ABSTRAcr.-In Superb Fairy-Wrens (Malurus cyaneus), groups of males cooperate with a single female to rear young, yet offspring are usually sired by males from outside the group. In this unusual mating system there is potential for intense sperm competition. During the breeding season, males develop a sperm storage structure (cloacal protuberance) and testes that proportionally are among the largest found in passerines. We compared the development pattern and size of cloacal protuberances of males differing in age and social status. Protuberance size increased with body mass. Age, intragroup dominance, and pairing status did not influence the overall size of the protuberance, but old males had a larger tip on their protuberance. This prominent tip has not been reported in other species, and we speculate that it serves as an intromittent organ. Other birds with large testes and cloacal protuberances have high copulation rates, but copulation in Superb Fairy-Wrens is only very rarely observed. We propose that the cloacal protuberance and large testes of Superb Fairy-Wrens provide large sperm reserves primarily for extrapair copulations. These may occur frequently, or involve the transfer of large ejaculates. Received 13 January 1993, accepted 14 March 1993.

Geographically pervasive effects of urban noise on frequency and syllable rate of songs and calls in silvereyes (Zosterops lateralis)

Recent studies in the Northern Hemisphere have shown that songbirds living in noisy urban environments sing at higher frequencies than their rural counterparts. However, several aspects of this phenomenon remain poorly understood. These include the geographical scale over which such patterns occur (most studies have compared local populations), and whether they involve phenotypic plasticity or microevolutionary change. We conducted a field study of silvereye (Zosterops lateralis) vocalizations over more than 1 million km2 of urban and rural south-eastern Australia, and compared possible effects of urban noise on songs (which are learned) and contact calls (which are innate). Across 14 paired urban and rural populations, silvereyes consistently sang both songs and contact calls at higher frequencies in urban environments. Syllable rate (syllables per second) decreased in urban environments, consistent with the hypothesis that reflective structures degrade song and encourage longer intervals between syllables. This comprehensive study is, to our knowledge, the first to demonstrate varied adaptations of urban bird vocalizations over a vast geographical area, and to provide insight into the mechanism responsible for these changes.

Natal and breeding dispersal in a co-operative, extra-group-mating bird

Natal and breeding dispersal of yearling and adult Superb Fairy-wrens Malurus cyaneus were studied for five years in Canberra, Australia. Superb Fairy-wrens are co-operative breeders and exhibit male philopatry and female-biased dispersal. Dispersal by yearling males was prompted mainly by breeding vacancies in nearby territories, and most males acquired a social mate without leaving their natal territory. All females dispersed in their first year, in two discrete phases. Early dispersal by females appears to be volitional, whereas late dispersal is forced by aggression by mothers. Early-dispersing females fledged earlier and dispersed further than latedispersing females. Females travelled further than males, and either gained a breeding position at age one year, or disappeared. Obligate dispersal by young females appears to be costly, contradicting predictions of philopatry by co-operative breeding theory. Dispersal by established breeders was uncommon, and was female-biased. The role of the unusual mating system of the species is discussed, and dispersal patterns in this species are compared and contrasted with those of its congener M. splendens.

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 FST 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 FST. 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.

Brood Parasitism and the Evolution of Cooperative Breeding in Birds

Power in Numbers Avian brood parasites target particular bird species to raise their offspring, sometimes at great cost to the foster family. Feeney et al. (p. 1506; see the Perspective by Spottiswoode) analyzed the global distribution of brood parasitism and found a correlation with the occurrence of cooperative breeders across multiple taxa. For example, Australian fairy wrens breed both singly and in cooperative groups, but the group breeders are better able to resist parasites than lone pairs, indicating that the prevalence of cooperative breeding may be a response to brood parasites. The skewed global distribution of cooperatively breeding birds may result from their coevolution with brood parasites. [Also see Perspective by Spottiswoode] The global distribution of cooperatively breeding birds is highly uneven, with hotspots inAustralasia and sub-Saharan Africa. The ecological drivers of this distribution remain enigmatic yet could yield insights into the evolution and persistence of cooperative breeding. We report that the global distributions of avian obligate brood parasites and cooperatively breeding passerines are tightly correlated and that the uneven phylogenetic distribution of cooperative breeding is associated with the uneven targeting of hosts by brood parasites. With a long-term field study, we show that brood parasites can acquire superior care for their young by targeting cooperative breeders. Conversely, host defenses against brood parasites are strengthened by helpers at the nest. Reciprocally selected interactions between brood parasites and cooperative breeders may therefore explain the close association between these two breeding systems.

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.