Nestling Begging Calls Resemble Maternal Vocal Signatures When Mothers Call Slowly to Embryos.

AbstractVocal production learning (the capacity to learn to produce vocalizations) is a multidimensional trait that involves different learning mechanisms during different temporal and socioecological contexts. Key outstanding questions are whether vocal production learning begins during the embryonic stage and whether mothers play an active role in this through pupil-directed vocalization behaviors. We examined variation in vocal copy similarity (an indicator of learning) in eight species from the songbird family Maluridae, using comparative and experimental approaches. We found that (1) incubating females from all species vocalized inside the nest and produced call types including a signature "B element" that was structurally similar to their nestlings' begging call; (2) in a prenatal playback experiment using superb fairy wrens (Malurus cyaneus), embryos showed a stronger heart rate response to playbacks of the B element than to another call element (A); and (3) mothers that produced slower calls had offspring with greater similarity between their begging call and the mother's B element vocalization. We conclude that malurid mothers display behaviors concordant with pupil-directed vocalizations and may actively influence their offspring's early life through sound learning shaped by maternal call tempo.

Best of both worlds? Helpers in a cooperative fairy-wren assist most to breeding pairs that comprise a potential mate and a relative.

In cooperative breeders, individuals forego independent reproduction and help others raise offspring. Helping is proposed to be driven by indirect benefits from raising relatives, and/or direct benefits from raising additional recruits or helping itself. We propose that consideration of social context is also important, in particular the characteristics of the breeding pair: helping may also serve to lighten the workload of-or maintain social bonds with-breeders (e.g. kin, potential mates) who in turn can offer benefits to helpers (e.g. prolonged nepotism, future mating, future production of relatives). Here, we test this hypothesis, while controlling for potential direct and indirect benefits from raising offspring, in purple-crowned fairy-wrens (Malurus coronatus) exhibiting variation in social group composition, and thus, breeder value. We show that helper provisioning rates to the nest were explained by characteristics of breeders that helpers assisted, rather than benefits from raising offspring. The presence of at least one related breeder was a prerequisite to help, but helpers provisioned most if assisting a relative and potential mate. Neglecting to take group composition into account would have led to misinterpretation of our results. A comprehensive understanding of the evolution of cooperative breeding hence requires nuanced consideration of social context.

Hot and dry conditions predict shorter nestling telomeres in an endangered songbird: Implications for population persistence.

Climate warming is increasingly exposing wildlife to sublethal high temperatures, which may lead to chronic impacts and reduced fitness. Telomere length (TL) may link heat exposure to fitness, particularly at early-life stages, because developing organisms are especially vulnerable to adverse conditions, adversity can shorten telomeres, and TL predicts fitness. Here, we quantify how climatic and environmental conditions during early life are associated with TL in nestlings of wild purple-crowned fairy-wrens (Malurus coronatus), endangered songbirds of the monsoonal tropics. We found that higher average maximum air temperature (range 31 to 45 °C) during the nestling period was associated with shorter early-life TL. This effect was mitigated by water availability (i.e., during the wet season, with rainfall), but independent of other pertinent environmental conditions, implicating a direct effect of heat exposure. Models incorporating existing information that shorter early-life TL predicts shorter lifespan and reduced fitness showed that shorter TL under projected warming scenarios could lead to population decline across plausible future water availability scenarios. However, if TL is assumed to be an adaptive trait, population viability could be maintained through evolution. These results are concerning because the capacity to change breeding phenology to coincide with increased water availability appears limited, and the evolutionary potential of TL is unknown. Thus, sublethal climate warming effects early in life may have repercussions beyond individual fitness, extending to population persistence. Incorporating the delayed reproductive costs associated with sublethal heat exposure early in life is necessary for understanding future population dynamics with climate change.

Telomere length declines with age, but relates to immune function independent of age in a wild passerine.

Telomere length (TL) shortens with age but telomere dynamics can relate to fitness components independent of age. Immune function often relates to such fitness components and can also interact with telomeres. Studying the link between TL and immune function may therefore help us understand telomere-fitness associations. We assessed the relationships between erythrocyte TL and four immune indices (haptoglobin, natural antibodies (NAbs), complement activity (CA) and heterophil-lymphocyte (HL) ratio; n = 477-589), from known-aged individuals of a wild passerine (Malurus coronatus). As expected, we find that TL significantly declined with age. To verify whether associations between TL and immune function were independent of parallel age-related changes (e.g. immunosenescence), we statistically controlled for sampling age and used within-subject centring of TL to separate relationships within or between individuals. We found that TL positively predicted CA at the between-individual level (individuals with longer average TL had higher CA), but no other immune indices. By contrast, age predicted the levels of NAbs and HL ratio, allowing inference that respective associations between TL and age with immune indices are independent. Any links existing between TL and fitness are therefore unlikely to be strongly mediated by innate immune function, while TL and immune indices appear independent expressions of individual heterogeneity.

No Evidence for Constitutive Innate Immune Senescence in a Longitudinal Study of a Wild Bird.

AbstractAging is associated with declines in physiological performance; declining immune defenses particularly could have consequences for age-related fitness and survival. In aging vertebrates, adaptive (memory-based) immune responses typically become impaired, innate (nonspecific) responses undergo lesser declines, and inflammation increases. Longitudinal studies of immune functions in wild animals are rare, yet they are needed to understand immunosenescence under evolutionarily relevant conditions. Using longitudinal data from a tropical passerine (Malurus coronatus) population, we investigate how population trends emerge from within-individual changes and between-individual heterogeneity (e.g., selective disappearance) in immune status. We quantified constitutive immune indexes (haptoglobin [inflammation associated], natural antibodies, complement [lytic] activity, and heterophil-lymphocyte ratio; n=505-631) in individuals sampled one to seven times over 5 yr. Unexpectedly, longitudinal analyses showed no age-related change within individuals in any immune index, despite sufficient power to detect within-individual change. Between individuals, we found age-related declines in natural antibodies and increases in heterophil-lymphocyte ratios. However, selective disappearance could not adequately explain between-individual age effects, and longitudinal models could not explain our data better than cross-sectional analyses. The lack of clear within-individual immunosenescence is itself notable. Persistent levels of haptoglobin, complement activity, and natural antibodies into old age suggests that these immune components are maintained, potentially with adaptive significance.

Telomere dynamics in the first year of life, but not later in life, predict lifespan in a wild bird.

Telomeres are protective, nucleoprotein structures at the end of chromosomes that have been associated with lifespan across taxa. However, the extent to which these associations can be attributed to absolute length vs. the rate of telomere shortening prior to sampling remains unresolved. In a longitudinal study, we examined the relationship between lifespan, telomere length and the rate of telomere shortening in wild, purple-crowned fairy-wrens (Malurus coronatus coronatus). To this end, we measured telomere length using quantitative polymerase chain reaction in the blood of 59 individuals sampled as nestlings and 4-14 months thereafter, and in 141 known-age individuals sampled on average three times across adulthood. We applied within-subject centring analyses to simultaneously test for associations between lifespan and average telomere length and telomere shortening. We reveal that the rate of telomere shortening and to a lesser extent telomere length in the first year of life independently predicted lifespan, with individuals with faster shortening rates and/or shorter telomeres living less long. In contrast, in adulthood neither telomere shortening nor telomere length predicted lifespan, despite a considerably larger data set. Our results suggest that telomere length measured very early in life (during development) and longitudinal assessments of telomere shortening during the first year of life constitute more useful biomarkers of total life expectancy than either telomere length measured after development, or telomere shortening later in adulthood.

Context-dependent social benefits drive cooperative predator defense in a bird.

Understanding the major evolutionary transition from solitary individuals to complex societies is hampered by incomplete insight into the drivers of living in cooperative groups.1-3 This may be because the benefits of sociality can derive from group living itself (e.g., dilution of predation risk),4,5 or depend on social context (e.g., kin or potential mates represent beneficial group members).6-8 Cooperative breeders, where non-breeding subordinates assist breeders, have provided important insights into the drivers of cooperation, but comprehensive assessment of diverse potential benefits has been hindered by a prevailing focus on benefits deriving from raising offspring.9-11 We propose a novel paradigm to tease apart different benefits by comparing cooperative responses to predators threatening dependent young and adult group members according to their value for the responding individual. Applying this approach in purple-crowned fairy-wrens, Malurus coronatus, we show that non-breeding subordinates are more responsive to nest predators-a threat to offspring-when their probability of inheriting a breeding position is greater-irrespective of group size, relatedness to offspring, or opportunity to showcase individual quality to potential mates. This suggests that offspring defense is modulated according to the benefits of raising future helpers. Conversely, when predators pose a threat to adults, responsiveness depends on social context: subordinates respond more often when kin or potential mates are under threat, or when group members are associated with mutualistic social bonds, indirect genetic benefits, and future reproductive benefits.9,12,13 Our results demonstrate that direct and kin-selected benefits of sociality are context dependent, and highlight the importance of predation risk in driving complex sociality.

Fitness outcomes in relation to individual variation in constitutive innate immune function.

Although crucial for host survival when facing persistent parasite pressure, costly immune functions will inevitably compete for resources with other energetically expensive traits such as reproduction. Optimizing, but not necessarily maximizing, immune function might therefore provide net benefit to overall host fitness. Evidence for associations between fitness and immune function is relatively rare, limiting our potential to understand ultimate fitness costs of immune investment. Here, we assess how measures of constitutive immune function (haptoglobin, natural antibodies, complement activity) relate to subsequent fitness outcomes (survival, reproductive success, dominance acquisition) in a wild passerine (Malurus coronatus). Surprisingly, survival probability was not positively linearly predicted by any immune index. Instead, both low and high values of complement activity (quadratic effect) were associated with higher survival, suggesting that different immune investment strategies might reflect a dynamic disease environment. Positive linear relationships between immune indices and reproductive success suggest that individual heterogeneity overrides potential resource reallocation trade-offs within individuals. Controlling for body condition (size-adjusted body mass) and chronic stress (heterophil-lymphocyte ratio) did not alter our findings in a sample subset with available data. Overall, our results suggest that constitutive immune components have limited net costs for fitness and that variation in immune maintenance relates to individual differences more closely.

Short-Term Climate Variation Drives Baseline Innate Immune Function and Stress in a Tropical Bird: A Reactive Scope Perspective.

Investment in immune function can be costly, and life-history theory predicts trade-offs between immune function and other physiological demands. Environmental heterogeneity may constrain or change the optimal strategy and thereby alter baseline immune function (possibly mediated by stress responses). We tested several hypotheses relating variation in climatic, ecological, and social environments to chronic stress and levels of baseline innate immunity in a wild, cooperatively breeding bird, the purple-crowned fairy-wren (Malurus coronatus coronatus). From samples collected biannually over 5 yr, we quantified three indexes of constitutive innate immune function (haptoglobin/PIT54, natural antibodies, complement activity) and one index of chronic stress (heterophil-lymphocyte ratio; n=513-647 ). Using an information-theoretic and multimodel inference statistical approach, we found that habitat quality and social group size did not affect any immune index, despite hypothesized links to resource abundance and parasite pressure. Rather, short-term variation in temperature and rainfall was related to immune function, while overall differences between seasons were small or absent, despite substantial seasonal variation in climate. Contrary to our expectation, we found no evidence that physiological stress mediated any effects of short-term climatic variables on immune indexes, and alternative mechanisms may be involved. Our results may be interpreted from the perspective of reactive scope models, whereby predictive homeostasis maintains standing immune function relative to long-term demands, while short-term environmental change, being less predictable, has a greater influence on baseline immune function.

Early-life telomere length predicts lifespan and lifetime reproductive success in a wild bird.

Poor conditions during early development can initiate trade-offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life-history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early-life conditions to lifespan and fitness. In wild purple-crowned fairy-wrens, we combined measurements of nestling telomere length (TL) with detailed life-history data to investigate whether early-life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age-dependent with early-life TL having a positive effect on lifespan only among individuals that survived their first year. Early-life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early-life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early-life TL, which reflects growth, accumulated early-life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early-life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early- and late-life performance and trade-offs across a lifetime.

From ornament to armament or loss of function? Breeding plumage acquisition in a genetically monogamous bird.

The evolution of conspicuous male traits is thought to be driven by female mate choice or male-male competition. These two mechanisms are often viewed as distinct processes, with most studies focusing on female choice. However, both mechanisms of sexual selection can act simultaneously on the same trait (i.e., dual function) and/or interact in a synergistic or conflicting way. Dual-function traits are commonly assumed to originate through male-male competition before being used in female choice; yet, most studies focusing on such traits could not determine the direction of change, lacking phylogenetic information. We investigated the role of conspicuous male seasonal plumage in male-male competitive interactions in the purple-crowned fairy-wren Malurus coronatus, a cooperatively breeding bird. Male breeding plumage in most Malurus species is selected by female choice through extra-pair mate choice, but unlike its congeners, M. coronatus is genetically monogamous, and females do not seem to choose males based on breeding plumage acquisition. Our study shows that, within groups, subordinate males that were older, and therefore higher-ranked in the queue for breeder position inheritance, produced a more complete breeding plumage. In line with this, subordinate males that were older and/or displayed a more complete breeding plumage were more successful in competitively acquiring a breeder position. A role as a signal of competitive ability was experimentally confirmed by presenting models of males: in breeding colours, these received more aggression from resident breeder males than in nonbreeding colours, but elicited limited response from females, consistent with competitors in breeding plumage being perceived as a bigger threat to the breeder male. The role of the conspicuous breeding plumage in mediating male-male interactions might account for its presence in this genetically monogamous species. As phylogenetic reconstructions suggest a past female choice function in M. coronatus, this could represent a sexual trait that shifted functions, or a dual-function trait that lost one function. These evolutionary scenarios imply that intra- and intersexual functions of ornaments may be gained or lost independently and offer new perspectives in understanding the complex dynamics of sexual selection.

Bright birds are cautious: seasonally conspicuous plumage prompts risk avoidance by male superb fairy-wrens.

Increased predation risk is considered a cost of having conspicuous colours, affecting the anti-predator behaviour of colourful animals. However, this is difficult to test, as individual factors often covary with colour and behaviour. We used alarm call playback and behavioural observations to assess whether individual birds adjust their response to risk according to their plumage colour. Male superb fairy-wrens (Malurus cyaneus) change from a dull brown to conspicuous blue plumage each year, allowing the behaviour of different coloured birds to be compared while controlling for within-individual effects. Because the timing of colour change varies among males, blue and brown birds can also be compared at the same time of year, controlling for seasonal effects on behaviour. While blue, fairy-wrens fled more often in response to alarm calls, and took longer to emerge from cover. Blue fairy-wrens also spent more time foraging in cover and being vigilant. Group members appeared to benefit from the presence of blue males, as they reduced their response to alarms, and allocated less time to sentinel behaviour when a blue male was close by. We suggest that fairy-wrens perceive themselves to be at a higher risk of predation while in conspicuous plumage and adjust their behaviour accordingly.