Aging and Senescence across Reproductive Traits and Survival in Superb Fairy-Wrens (Malurus cyaneus).

AbstractWhy do senescence rates of fitness-related traits often vary dramatically? By considering the full aging trajectories of multiple traits, we can better understand how a species' life history shapes the evolution of senescence within a population. Here, we examined age-related changes in sex-specific survival, reproduction, and several components of reproduction using a long-term study of a cooperatively breeding songbird, the superb fairy-wren (Malurus cyaneus). We compared aging patterns between traits by estimating standardized rates of maturation, age of onset of senescence, and rates of senescence while controlling for confounding factors reflecting individual variability in life history. We found striking differences in aging and senescence patterns between survival and reproduction as well as between reproductive traits. In both sexes, survival started to decline from maturity onward. In contrast, all reproductive traits showed improvements into early adulthood, and many showed little or no evidence of senescence. In females, despite senescence in clutch size, number of offspring surviving to independence did not decline in late life, possibly due to improvements in maternal care with age. Superb fairy-wrens have exceptionally high levels of extragroup paternity, and while male within-group reproductive success did not change with age, extragroup reproductive success showed a dramatic increase in early ages, followed by a senescent decline, suggesting that male reproductive aging is driven by sexual selection. We discuss how the superb fairy-wrens' complex life history may contribute to the disparate aging patterns across different traits.

When to start and when to stop: Effects of climate on breeding in a multi-brooded songbird.

Climate warming has been shown to affect the timing of the onset of breeding of many bird species across the world. However, for multi-brooded species, climate may also affect the timing of the end of the breeding season, and hence also its duration, and these effects may have consequences for fitness. We used 28 years of field data to investigate the links between climate, timing of breeding, and breeding success in a cooperatively breeding passerine, the superb fairy-wren (Malurus cyaneus). This multi-brooded species from southeastern Australia has a long breeding season and high variation in phenology between individuals. By applying a "sliding window" approach, we found that higher minimum temperatures in early spring resulted in an earlier start and a longer duration of breeding, whereas less rainfall and more heatwaves (days > 29°C) in late summer resulted in an earlier end and a shorter duration of breeding. Using a hurdle model analysis, we found that earlier start dates did not predict whether or not females produced any young in a season. However, for successful females who produced at least one young, earlier start dates were associated with higher numbers of young produced in a season. Earlier end dates were associated with a higher probability of producing at least one young, presumably because unsuccessful females kept trying when others had ceased. Despite larger scale trends in climate, climate variables in the windows relevant to this species' phenology did not change across years, and there were no temporal trends in phenology during our study period. Our results illustrate a scenario in which higher temperatures advanced both start and end dates of individuals' breeding seasons, but did not generate an overall temporal shift in breeding times. They also suggest that the complexity of selection pressures on breeding phenology in multi-brooded species may have been underestimated.

Contrasting effects of climate on juvenile body size in a Southern Hemisphere passerine bird.

Despite extensive research on the topic, it has been difficult to reach general conclusions as to the effects of climate change on morphology in wild animals: in particular, the effects of warming temperatures have been associated with increases, decreases or stasis in body size in different populations. Here, we use a fine-scale analysis of associations between weather and offspring body size in a long-term study of a wild passerine bird, the cooperatively breeding superb fairy-wren, in south-eastern Australia to show that such variation in the direction of associations occurs even within a population. Over the past 26 years, our study population has experienced increased temperatures, increased frequency of heatwaves and reduced rainfall - but the mean body mass of chicks has not changed. Despite the apparent stasis, mass was associated with weather across the previous year, but in multiple counteracting ways. Firstly, (i) chick mass was negatively associated with extremely recent heatwaves, but there also positive associations with (ii) higher maximum temperatures and (iii) higher rainfall, both occurring in a period prior to and during the nesting period, and finally (iv) a longer-term negative association with higher maximum temperatures following the previous breeding season. Our results illustrate how a morphological trait may be affected by both short- and long-term effects of the same weather variable at multiple times of the year and that these effects may act in different directions. We also show that climate within the relevant time windows may not be changing in the same way, such that overall long-term temporal trends in body size may be minimal. Such complexity means that analytical approaches that search for a single 'best' window for one particular weather variable may miss other relevant information, and is also likely to make analyses of phenotypic plasticity and prediction of longer-term population dynamics difficult.

Winter mortality of a passerine bird increases following hotter summers and during winters with higher maximum temperatures.

Climate change may influence animal population dynamics through reproduction and mortality. However, attributing changes in mortality to specific climate variables is challenging because the exact time of death is usually unknown in the wild. Here, we investigated climate effects on adult mortality in Australian superb fairy-wrens (Malurus cyaneus). Over a 27-year period, mortality outside the breeding season nearly doubled. This nonbreeding season mortality increased with lower minimum (night-time) and higher maximum (day-time) winter temperatures and with higher summer heat wave intensity. Fine-scale analysis showed that higher mortality in a given week was associated with higher maxima 2 weeks prior and lower minima in the current fortnight, indicating costs of temperature drops. Increases in summer heat waves and in winter maximum temperatures collectively explained 62.6% of the increase in mortality over the study period. Our results suggest that warming climate in both summer and winter can adversely affect survival, with potentially substantial population consequences.

Fluctuations in population composition dampen the impact of phenotypic plasticity on trait dynamics in superb fairy-wrens.

1. In structured populations, phenotypic change can result from changes throughout an individual's lifetime (phenotypic plasticity, age-related changes), selection and changes in population composition (environment- or density-driven fluctuations in age-structure). 2. The contribution of population dynamics to phenotypic change has often been ignored. However, for understanding trait dynamics, it is important to identify both the individual- and population-level mechanisms responsible for trait change, because they potentially reinforce or counteract each other. 3. We use 22 years of field data to investigate the dynamics of a sexually selected phenological trait, the timing of nuptial moult in superb fairy-wrens Malurus cyaneus. 4. We show that trait expression is both climate- and age-dependent, but that phenotypic plasticity in response to climate variability also varies with age. Old males can acquire nuptial plumage very early after high rainfall, but 1- to 2-year-olds cannot. However, males of all ages that defer moult to later in the year acquire nuptial plumage earlier when conditions are warmer. 5. The underlying mechanism appears to be that old males may risk moulting in the most challenging period of the year: in autumn, when drought restricts food abundance and during the cold winter. By contrast, young males always moult during the spring transition to benign - warmer and generally wetter - conditions. Temperature changes dominate this transition that heralds the breeding season, thereby causing both young and late-moulting older birds to be temperature sensitive. 6. Climate and age also affect trait dynamics via a population dynamical pathway. The same high rainfall that triggers early moulting in old males concurrently increases offspring recruitment and thereby reduces the average age of males in the population. Consequently, effects of rainfall on trait dynamics through phenotypic plasticity of old males are dampened by synchronous rejuvenation of the age-structure. 7. A long-term trend towards drier environments prompted phenotypic change because of plasticity, but this was masked by climate-driven demographic change (causing apparent stasis). This suggests a novel explanation for why trait change may fail to reflect the observed pattern of directional selection or phenotypic plasticity.

Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.

The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

hiphop: Improved paternity assignment among close relatives using a simple exclusion method for biallelic markers.

Assignment of parentage with molecular markers is most difficult when the true parents have close relatives in the adult population. Here, we present an efficient solution to that problem by extending simple exclusion approaches to parentage analysis with single nucleotide polymorphic markers (SNPs). We augmented the previously published homozygote opposite test (hot), which counts mismatches due to the offspring and candidate parent having different homozygous genotypes, with an additional test. In this case, parents homozygous for the same SNP are incompatible with heterozygous offspring (i.e., "Homozygous Identical Parents, Heterozygous Offspring are Precluded": hiphop). We tested this approach in a cooperatively breeding bird, the superb fairy-wren, Malurus cyaneus, where rates of extra-pair paternity are exceptionally high, and where paternity assignment is challenging because breeding males typically have first-order adult relatives in their neighbourhood. Combining the tests and conditioning on the maternal genotype with a set of 1376 autosomal SNPs always allowed us to distinguish a single most likely sire from his relatives, and also to identify cases where the true sire must have been unsampled. In contrast, if just the hot test was used, we failed to identify a single most-likely sire in 2.5% of cases. Resampling enabled us to create guidelines for the number of SNPs required when first-order relatives coexist in the mating pool. Our method, implemented in the R package hiphop, therefore provides unambiguous parentage assignments even in systems with complex social organisation. We also identified a suite of Z- and W-linked SNPs that always identified sex correctly.

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.

Demography of male reproductive queues in cooperatively breeding superb fairy-wrens Malurus cyaneus.

1. Subordinate helpers in cooperative societies may gain both immediate and future benefits, including paternity and territorial inheritance. However, if such opportunities correlate with rank in the queue, it is unclear why such queues should be stable. 2. In cooperatively breeding superb fairy-wrens Malurus cyaneus, only males are generally philopatric, and form stable hierarchical queues for the dominant position. 3. Male opportunities for reproduction are influenced both by their dominance status within the group, and their relatedness to the breeding female. For young queuing subordinates, the breeding female is typically their mother. Because of incest avoidance, reproduction is possible only through extra-group mating, even if the dominant position is achieved while the mother is still on the territory. If the mother dies while the helper is still a subordinate, he can seek matings both outside the group, and with the unrelated replacement female within the group. Finally, males can achieve the dominant position and pair with an unrelated female by inheritance, dispersal to a neighbouring vacancy, or by forming a liaison with an immigrant subordinate female that causes fission of the natal territory. 4. On average males spent more time living with unrelated females than with their mother. Subordinate males gained no survival advantages when living with their mother rather than an unrelated female, contrary to the prediction that parents facilitate the survival of their offspring. 5. Dominants and subordinates also had similar survival. Mortality accelerated over time, probably because older males invest more in extra-group courtship display. 6. Fairy-wren queues are likely to be stable because older birds are superior, and because extra-pair mating provides direct benefits to subordinates.

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.

Inbreeding, inbreeding depression, and infidelity in a cooperatively breeding bird.

Inbreeding depression plays a major role in shaping mating systems: in particular, inbreeding avoidance is often proposed as a mechanism explaining extra-pair reproduction in socially monogamous species. This suggestion relies on assumptions that are rarely comprehensively tested: that inbreeding depression is present, that higher kinship between social partners increases infidelity, and that infidelity reduces the frequency of inbreeding. Here, we test these assumptions using 26 years of data for a cooperatively breeding, socially monogamous bird with high female infidelity, the superb fairy-wren (Malurus cyaneus). Although inbred individuals were rare (∼6% of offspring), we found evidence of inbreeding depression in nestling mass (but not in fledgling survival). Mother-son social pairings resulted in 100% infidelity, but kinship between a social pair did not otherwise predict female infidelity. Nevertheless, extra-pair offspring were less likely to be inbred than within-pair offspring. Finally, the social environment (the number of helpers in a group) did not affect offspring inbreeding coefficients or inbreeding depression levels. In conclusion, despite some agreement with the assumptions that are necessary for inbreeding avoidance to drive infidelity, the apparent scarcity of inbreeding events and the observed levels of inbreeding depression seem insufficient to explain the ubiquitous infidelity in this system, beyond the mother-son mating avoidance.