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.

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.

Variability, heritability and condition-dependence of the multidimensional male colour phenotype in a passerine bird.

Elaborate ornamental traits are commonly assumed to be honest signals of individual quality, owing to the presumed costs involved in their production and/or maintenance. Such traits are often highly variable, possibly because of condition-dependence and/or high underlying genetic variation, and it has been suggested that their expression should be more sensitive to condition and/or more heritable than non-ornamental traits. Many bird species display colourful plumage with multiple distinct patches of different developmental origins, forming complex colour phenotypes. Despite this complexity, colourful ornaments are often studied in isolation, without comparison to suitable non-ornamental controls. Based on plumage reflectance data collected over 8 years, we assessed the signalling potential of the multidimensional male colour phenotype in a tropical bird: the purple-crowned fairy-wren Malurus coronatus. Specifically, we tested the predictions that the expression of putative ornamental colours (purple and black - the breeding colours - and blue) is (1) more variable, (2) more heritable and (3) more condition-dependent compared to year-round non-ornamental colours (buff-white and brown). Our results show that ornamental colours exhibit greater levels of variability, and some chromatic components of purple and blue colouration appear slightly heritable (h² = 0.19-0.30). However, contrary to predictions of heightened condition-dependence in ornaments, only brightness of the buff-white and brown colouration increased with male body condition, although brightness of the purple colouration was related to male age as expected. Despite partial support for predictions, the lack of consistent patterns illustrates the complexity of visual signals and highlights the need to study colour phenotypes in their entirety.

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.

BDNF-dependent plasticity induced by peripheral inflammation in the primary sensory and the cingulate cortex triggers cold allodynia and reveals a major role for endogenous BDNF as a tuner of the affective aspect of pain.

Painful experiences are multilayered, composed of sensory, affective, cognitive and behavioral facets. Whereas it is well accepted that the development of chronic pain is due to maladaptive neuronal changes, the underlying molecular mechanisms, their relationship to the different pain modalities, and indeed the localization of these changes are still unknown. Brain-derived neurotrophic factor (BDNF) is an activity-dependent neuromodulator in the adult brain, which enhances neuronal excitability. In the spinal cord, BDNF underlies the development and maintenance of inflammatory and neuropathic pain. Here, we hypothesized that BDNF could be a trigger of some of these plastic changes. Our results demonstrate that BDNF is upregulated in the anterior cingulate cortex (ACC) and the primary sensory cortex (S1) in rats with inflammatory pain. Injections of recombinant BDNF (into the ACC) or a viral vector synthesizing BDNF (into the ACC or S1) triggered both neuronal hyperexcitability, as shown by elevated long-term potentiation, and sustained pain hypersensitivity. Finally, pharmacological blockade of BDNF-tropomyosin receptor kinase B (TrkB) signaling in the ACC, through local injection of cyclotraxin-B (a novel, highly potent, and selective TrkB antagonist) prevented neuronal hyperexcitability, the emergence of cold hypersensitivity, and passive avoidance behavior. These findings show that BDNF-dependent neuronal plasticity in the ACC, a structure known to be involved in the affective-emotional aspect of pain, is a key mechanism in the development and maintenance of the emotional aspect of chronic pain.

Cyclic colour change in the bearded dragon Pogona vitticeps under different photoperiods.

The ability to change colour rapidly is widespread among ectotherms and has various functions including camouflage, communication and thermoregulation. The process of colour change can occur as an aperiodic event or be rhythmic, induced by cyclic environmental factors or regulated by internal oscillators. Despite the importance of colour change in reptile ecology, few studies have investigated the occurrence of a circadian rhythm in lizard pigmentation. Additionally, although colour change also entails changes in near-infrared reflectance, which may affect thermoregulation, little research has examined this part of the spectrum. We tested whether the bearded dragon lizard, Pogona vitticeps, displays an endogenous circadian rhythm in pigmentation changes that could be entrained by light/dark (LD) cycles and how light affected the relative change in reflectance in both ultraviolet-visible and near-infrared spectra. We subjected 11 lizards to four photoperiodic regimens: LD 12:12; LD 6:18; LD 18:6 and DD; and measured their dorsal skin reflectance at 3-hour intervals for 72 hours after a habituation period. A proportion of lizards displayed a significant rhythm under constant darkness, with maximum reflectance occurring in the subjective night. This endogenous rhythm synchronised to the different artificial LD cycles, with maximum reflectance occurring during dark phases, but did not vary in amplitude. In addition, the total ultraviolet-visible reflectance in relation to the total near-infrared reflectance was significantly higher during dark phases than during light phases. We conclude that P. vitticeps exhibits a circadian pigmentation rhythm of constant amplitude, regulated by internal oscillators and that can be entrained by light/dark cycles.