Michael C. Double

Pre–dawn infidelity: females control extra-pair mating in superb fairy–wrens

Despite great interest in the use of extra–pair mating as a tool for examining female choice and intersexual selection, the underlying assumption of female control has proved difficult to verify empirically. We combined microsatellite genotyping and radiotelemetry of fertile females in order to investigate mate choice in superb fairy–wrens Malurus cyaneus, the bird with the highest known rate of extra–pair fertilization. All five females radio tracked during the peak of fertility, two to four days before the first egg is laid, undertook pre–dawn forays. All extra–pair young produced by the female were sired by a male visited during their forays, indicating that females control extra–pair fertilizations. In a larger sample of paternity data, some broods were sired by two extra–group males. In virtually all the cases the territory of the two sires were on an identical linear trajectory from the females territory. This again suggests that extra–group paternity in superb fairy–wrens is directly linked to female extra–territorial forays. In other species mixed paternity has been taken to indicate that females attempt to insure against infertile pairings or try to maximize the genetic diversity of their brood. However, in fairy–wrens the likelihood of multiple extra–group paternity increased greatly as females traversed more territories in order to mate, perhaps suggesting that females which foray further are more likely to have difficulties locating the preferred male.

DISPERSAL, PHILOPATRY, AND INFIDELITY: DISSECTING LOCAL GENETIC STRUCTURE IN SUPERB FAIRY-WRENS (MALURUS CYANEUS)

Abstract Dispersal influences evolution, demography, and social characteristics but is generally difficult to study. Here we combine long‐term demographic data from an intensively studied population of superb fairy‐wrens(Malurus cyaneus) and multivariate spatial autocorrelation analyses of microsatellite genotypes to describe dispersal behavior in this species. The demographic data revealed: (1) sex‐biased dispersal: almost all individuals that dispersed into the study area over an eight‐year period were female (93%; n 5 153); (2) high rates of extragroup infidelity (66% of offspring), which also facilitated local gene dispersal; and (3) skewed lifetime reproductive success in both males and females. These data led to three expectations concerning the patterns of fine‐scale genetic structure: (1) little or no spatial genetic autocorrelation among females, (2) positive spatial genetic autocorrelation among males, and (3) a heterogeneous genetic landscape. Global autocorrelation analysis of the genotypes present in the study population confirmed the first two expectations. A novel two‐dimensional local autocorrelation analysis confirmed the third and provided new insight into the patterns of genetic structure across the two‐dimensional landscape. We highlight the potential of autocorrelation analysis to infer evolutionary processes but also emphasize that genetic patterns in space cannot be fully understood without an appropriate and intensive sampling regime and detailed knowledge of the individuals genotyped.

Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild

Females often mate with several males before producing offspring. Field studies of vertebrates suggest, and laboratory experiments on invertebrates confirm, that even when males provide no material benefits, polyandry can enhance offspring survival. This enhancement is widely attributed to genetic benefits that arise whenever paternity is biased towards males that sire more viable offspring. Field studies suggest that post-mating sexual selection biases fertilization towards genetically more compatible males and one controlled experiment has shown that, when females mate with close kin, polyandry reduces the relative number of inbred offspring. Another potential genetic benefit of polyandry is that it increases offspring survival because males with more competitive ejaculates sire more viable offspring. Surprisingly, however, there is no unequivocal evidence for this process. Here, by experimentally assigning mates to females, we show that polyandry greatly increases offspring survival in the Australian marsupial Antechinus stuartii. DNA profiling shows that males that gain high paternity under sperm competition sire offspring that are more viable. This beneficial effect occurs in both the laboratory and the wild. Crucially, there are no confounding non-genetic maternal effects that could arise if polyandry increases female investment in a particular reproductive event because A. stuartii is effectively semelparous. Our results therefore show that polyandry improves female lifetime fitness in nature. The threefold increase in offspring survival is not negated by a decline in maternal lifespan and is too large to be offset by an equivalent decline in the reproductive performance of surviving offspring.

Swingin' in the rain: condition dependence and sexual selection in a capricious world.

Signals used in mate attraction are predicted to be highly condition dependent, and thus should be sensitive to environmental contributions to condition. However, the effects of temporal fluctuations in the environment on sexual selection in long-lived animals have been largely ignored. Female superb fairy-wrens, Malurus cyaneus, use the time that males moult into nuptial plumage prior to the onset of the breeding season to distinguish between the extra-group sires that dominate paternity. Although moult varies predictably with age, and shows marked differences between males, the phenotypic distribution also changes radically with climate; so after dry summers few males can attempt early moult. We use the recently introduced de-lifing technique to examine sexual selection gradients over 15 years of selection. Overall, there was strong evidence of directional sexual selection for early moult. However, sexual selection was much stronger when the conditions were favourable (rainfall was high), and selection was undetectable in some years. The contribution of early moulting males to population growth increased when many males moulted early, decreased when early moulting males suffered disproportionate mortality and decreased when females lacked subordinate helpers, forcing them to cede paternity to their social partner. These data suggest that short-term and laboratory studies of mate choice and sexual selection may misrepresent or underestimate the complexity of the sexual selection landscape.

Genetic structure, conservation genetics and evidence of speciation by range expansion in shy and white-capped albatrosses.

Six variable microsatellite loci were used to examine genetic structuring in the closely related shy albatross (Thalassarche cauta) and white‐capped albatross (T. steadi). First, levels of genetic differentiation between the species, and among three populations within each species, were analysed using amova, FST and RST. We found high levels of genetic structuring and detected many unshared alleles between the species, which provide strong evidence against any contemporary gene flow between them. Within each species, shy albatross populations were found to be genetically distinct whereas white‐capped albatross populations were undifferentiated, which implies that dispersal events are much rarer in the former than in the latter. These results formed the basis for the recommendation that the three white‐capped albatross populations (as a whole) and each shy albatross population be treated as separate units for conservation. Second, levels of genetic diversity and allelic patterns in shy and white‐capped albatrosses were assessed for whether they support earlier mtDNA results suggesting that shy albatrosses arose through range expansion of white‐capped albatrosses. All measures indicated lower genetic diversity within shy albatrosses than within white‐capped albatrosses and upheld the hypothesis that shy albatrosses were founded by white‐capped albatrosses.

An unusual source of apparent mitochondrial heteroplasmy: duplicate mitochondrial control regions in Thalassarche albatrosses

Molecular ecologists, in search of suitable molecular markers, frequently PCR‐amplify regions of mitochondrial DNA from total DNA extracts. This approach, although common, is prone to the co‐amplification of nuclear copies of transposed DNA sequences (numts), which can then generate apparent mitochondrial sequence heteroplasmy. In this study we describe the discovery of apparent mitochondrial sequence heteroplasmy in Thalassarche albatrosses but eliminate the possibility of true sequence heteroplasmy and numts and instead reveal the source of the apparent heteroplasmy to be a duplicated control region. The two control regions align easily but are not identical in sequence or in length. Comparisons of functionally significant conserved sequence blocks do not provide evidence of degeneration in either duplicate. Phylogenetic analyses of domain I of both control region copies in five Thalassarche species indicate that they are largely evolving in concert; however, a short section within them is clearly evolving independently. To our knowledge this is the first time contrasting evolutionary patterns have been reported for duplicate control regions. Available evidence suggests that this duplication may be taxonomically widespread, so the results presented here should be considered in future evolutionary studies targeting the control region of all Procellariiformes and potentially other closely related avian groups.

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.

Subordinate superb fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males.

Explanations of cooperative breeding have largely focused on the indirect benefits philopatric offspring gain from investing in kin. However, recent molecular studies have revealed that in many species subordinates provision unrelated offspring. This has led to the re–evaluation of the direct and indirect benefits of helping behaviour. In this study, we used microsatellite genotyping to assess the extra–group reproductive success of subordinate superb fairy–wrens (Malurus cyaneus), a species with extremely high rates of extra–group paternity. Extra–group subordinate males sired 10.2% (193 out of 1895) of all offspring sampled between 1993 and 2000 and 21.4% (193 out of 901) of all illegitimate offspring sired by known males. The extra–group success of subordinates was greatly influenced by the attractiveness of their dominant male. Subordinates of attractive dominants sired more extra–group young than did average dominants. Evidence suggests that mate choice in superb fairy–wrens is error–prone and subordinates can gain direct reproductive benefits through parasitizing the reproductive success of attractive dominants.

Coalitions of relatives and reproductive skew in cooperatively breeding white-winged choughs

We used DNA fingerprinting to examine reproductive skew in cooperatively breeding white-winged choughs, Corcorax melanorhamphos, which live in groups of up to 20 individuals. Before a severe drought, groups that had been stable for multiple years were characterized by long-term monogamy involving a single breeding pair (high skew). After the drought, new groups formed from the amalgamation of multiple individuals and coalitions of relatives. At most one member of each faction succeeded in breeding, such that skew was dependent on the number of unrelated factions, and not group size. In the new groups, dominant males and females with supporting relatives were always successful. Whereas most females without support also gained breeding positions, many males without family support failed to breed. Thus subordinates gain indirect fitness by first helping related males to secure a breeding position, and then helping to raise their young. Our study demonstrates the advantage of operating in coalitions, and suggests that the acquisition of future allies may be a major benefit of helping behaviour in this species.

Exclusion probabilities for single‐locus paternity analysis when related males compete for matings

The statistical power of single‐locus paternity analyses has previously been assessed by calculating an expected exclusion probability (E), the probability of excluding a randomly chosen nonfather. This E‐statistic assumes that putative sires are a random selection of individuals from a panmictic study population. In species that display male natal philopatry, closely related individuals may be the principal competitors for paternity. In such structured populations, the E statistic will overestimate exclusion probability because males competing for paternity are more closely related than males chosen randomly from the population. A suite of loci thought to be sufficient for a panmictic population may frequently incorrectly assign paternity to close relatives of true sires. This study provides equations for calculating the expected probability of excluding a close male relative of the genetic sire (Erel) for any genotyping system that uses codominant markers. We also describe the use of Monte Carlo modelling to estimate exclusion probabilities when multiple male relatives compete for paternity. We show that the utility of a set of codominant markers will depend on the breeding behaviour and social system of the species in question.