Lifetime inclusive fitness effects of cooperative polygamy in the acorn woodpecker.

Although over 50 y have passed since W. D. Hamilton articulated kin selection and inclusive fitness as evolutionary explanations for altruistic behavior, quantifying inclusive fitness continues to be challenging. Here, using 30 y of data and two alternative methods, we outline an approach to measure lifetime inclusive fitness effects of cooperative polygamy (mate-sharing or cobreeding) in the cooperatively breeding acorn woodpecker Melanerpes formicivorus. For both sexes, the number of offspring (observed direct fitness) declined while the number of young parented by related cobreeders (observed indirect fitness effect) increased with cobreeding coalition size. Combining these two factors, the observed inclusive fitness effect of cobreeding was greater than breeding singly for males, while the pattern for females depended on whether fitness was age-weighted, as females breeding singly accrued greater fitness at younger ages than cobreeding females. Accounting for the fitness birds would have obtained by breeding singly, however, lifetime inclusive fitness effects declined with coalition size for males, but were greater for females breeding as duos compared to breeding singly, due largely to indirect fitness effects of kin. Our analyses provide a road map for, and demonstrate the importance of, quantifying indirect fitness as a powerful evolutionary force contributing to the costs and benefits of social behaviors.

Lifetime reproductive benefits of cooperative polygamy vary for males and females in the acorn woodpecker (Melanerpes formicivorus).

Cooperative breeding strategies lead to short-term direct fitness losses when individuals forfeit or share reproduction. The direct fitness benefits of cooperative strategies are often delayed and difficult to quantify, requiring data on lifetime reproduction. Here, we use a longitudinal dataset to examine the lifetime reproductive success of cooperative polygamy in acorn woodpeckers (Melanerpes formicivorus), which nest as lone pairs or share reproduction with same-sex cobreeders. We found that males and females produced fewer young per successful nesting attempt when sharing reproduction. However, males nesting in duos and trios had longer reproductive lifespans, more lifetime nesting attempts and higher lifetime reproductive success than those breeding alone. For females, cobreeding in duos increased reproductive lifespan so the lifetime reproductive success of females nesting in duos was comparable to those nesting alone and higher than those nesting in trios. These results suggest that for male duos and trios, reproductive success alone may provide sufficient fitness benefits to explain the presence of cooperative polygamy, and the benefits of cobreeding as a duo in females are higher than previously assumed. Lifetime individual fitness data are crucial to reveal the full costs and benefits of cooperative polygamy.

Habitat Saturation Results in Joint-Nesting Female Coalitions in a Social Bird.

Joint nesting by females and cooperative polyandry-cooperatively breeding groups with a male-biased breeder sex ratio-are little-understood, rare breeding systems. We tested alternative hypotheses of factors potentially driving these phenomena in a population of joint-nesting acorn woodpeckers (Melanerpes formicivorus). During periods of high population density and thus low independent breeding opportunities, acorn woodpecker females formed joint-nesting coalitions with close kin. Coalitions were typically associated with groups with a male bias. We found strong evidence for both inter- and intrasexual conflict, as joint nesting conferred a fitness benefit to some males, a significant fitness cost to females, and no gain in per capita reproductive output for either sex. Such conflict, particularly the cost to females, may be an important reason why joint nesting is rare among cooperatively breeding taxa.

Do avian blood parasites influence hypoxia physiology in a high elevation environment?

BACKGROUND: Montane birds which engage in elevational movements have evolved to cope with fluctuations in environmental hypoxia, through changes in physiological parameters associated with blood oxygen-carrying capacity such as haemoglobin concentration (Hb) and haematocrit (Hct). In particular, elevational migrants which winter at low elevations, encounter varying intensities of avian haemosporidian parasites as they traverse heterogeneous environments. Whilst high intensity parasite infections lead to anaemia, one can expect that the ability to cope with haemosporidian infections should be a key trait for elevational migrants that must be balanced against reducing the oxygen-carrying capacity of blood in response to high elevation. In this study, we explored the links between environmental hypoxia, migration, and disease ecology by examining natural variation in infections status and intensity of avian haemoporidians across a suite of Himalayan birds with different migratory strategies while controlling for host phylogeny. RESULTS: We found predictably large variation in haemoglobin levels across the elevational gradient and this pattern was strongly influenced by season and whether birds are elevational migrants. The overall malaria infection intensity declined with elevation whereas Hb and Hct decreased with increase in parasite intensity, suggesting an important role of malaria parasites on hypoxia stressed birds in high elevation environments. CONCLUSIONS: Our results provide a key insight into how physiological measures and sub-clinical infections might affect dynamics of high-elevation bird populations. We suggest a potential impact of avian elevational migration on disease dynamics and exposure to high intensity infections with disease spread in the face of climate change, which will exacerbate hypoxic stress and negative effects of chronic avian malaria infection on survival and reproductive success in wild birds. Future work on chronic parasite infections must consider parasite intensity, rather than relying on infection status alone.

Gazing Strategies among Sentinels of a Cooperative Breeder Are Repeatable but Unrelated to Survival.

Vigilance is a common behavioural adaptation to increase the chances of detecting predators before it is too late to escape. Behavioural traits are often repeatable among individuals over the long term, suggesting differences in personality. Earlier studies have documented individual consistency in the time allocated to vigilance. However, little is known about individual consistency in the ways vigilance is achieved from one moment to another and whether different patterns of vigilance among individuals are associated with survival. We aimed to determine whether sentinels of a cooperative breeder showed individual consistency in their vigilance and if individual variation was related to annual survival. During sentinel bouts from vantage points, Florida scrub-jays (Aphelocoma coerulescens) turn their heads from side to side to monitor their surroundings. Over three field seasons, we found that the head-turning frequency was repeatable in breeders but not in juveniles or non-breeding helpers. The moderate repeatability in breeders was not related to survival. Our results suggest that the head-turning frequency in sentinels of the Florida scrub-jay is repeatable in breeders but not in less experienced juveniles or helpers and, therefore, likely becomes more repeatable as individuals age. The assumption that individual variation in vigilance is related to survival was unsupported in our study and requires further study.

Multiple Sentinels in a Cooperative Breeder Synchronize Rather Than Coordinate Gazing.

Sentinels can detect predators and rivals early by monitoring their surroundings from vantage points. Multiple sentinels in a group may reduce the perceived predation risk by diluting the risk and increasing collective detection, especially if sentinels monitor different areas at the same time. We investigated sentinel behavior in groups of the Florida scrub jay (Aphelocoma caerulescens). Sentinels in this species turn their heads frequently to monitor different areas for threats. As predicted, we found that sentinels turned their heads less frequently in the presence of other sentinels. Multiple sentinels, however, tended to gaze in the same direction at the same time more often than predicted by chance alone. Gaze synchronization reduces the efficiency of collective detection by reducing visual coverage at any one time at the group level. Despite the benefits of the presence of other sentinels, our results highlight the limits to collective detection when multiple individuals are vigilant at the same time.

Acorn woodpecker movements and social networks change with wildfire smoke.

Climate change has contributed to increased wildfires1,2. Wildfire smoke exposes wildlife to hazards and mortality from particulate matter on a scale larger than the area impacted by fire3,4. Using automated radiotelemetry, we illustrate how smoky conditions are associated with changes in behavior of acorn woodpeckers (Melanerpes formicivorus), a flagship species of oak (Quercus spp.) savannas of western North America. On smoky days, birds spent more time at their home territory and reduced visitation to others, especially to distant territories. Associations between birds decreased, and individuals were less assorted by group in co-visitation networks, suggesting less inter-individual coordination on smoky days. We show that between 2016 and 2020, ∼14% of the acorn woodpecker population in the US experienced fire, potentially exposing on average 89.42% of the range to atmospheric smoke annually. These findings highlight how potential effects of smoke on animal behavior may be widespread and exacerbate negative impacts of increasingly common "megafires", even in fire-adapted ecosystems.

Variation in insulative feather structure in songbirds replacing each other along a tropical elevation gradient.

High-elevation organisms are expected to evolve physiological adaptations to cope with harsh environmental conditions. Yet, evidence for such adaptive differences, especially compared to closely related lowland taxa occurring along the same elevational gradient, is rare. Revisiting an anecdotal natural history observation by O. Bangs from 1899 and based on new measurements of museum specimens, we confirmed that the high-elevation hermit wood wren (Henicorhina anachoreta) from the Sierra Nevada de Santa Marta, Colombia, has longer, more insulative feathers on the chest and back, than its lower-elevation counterpart the grey-breasted wood wren (H. leucophrys). However, we did not find evidence for the same specializations in subspecies of H. leucophrys that live at high elevations on other elevational gradients in the Colombian Andes, although similar adaptive solutions have arisen in separate mountain systems like the Himalayas. Adaptations in plumage may be associated with the recurrence of elevational species replacements throughout the tropics.

Back to the Future: Reintegrating Biology to Understand How Past Eco-evolutionary Change Can Predict Future Outcomes.

During the last few decades, biologists have made remarkable progress in understanding the fundamental processes that shape life. But despite the unprecedented level of knowledge now available, large gaps still remain in our understanding of the complex interplay of eco-evolutionary mechanisms across scales of life. Rapidly changing environments on Earth provide a pressing need to understand the potential implications of eco-evolutionary dynamics, which can be achieved by improving existing eco-evolutionary models and fostering convergence among the sub-fields of biology. We propose a new, data-driven approach that harnesses our knowledge of the functioning of biological systems to expand current conceptual frameworks and develop corresponding models that can more accurately represent and predict future eco-evolutionary outcomes. We suggest a roadmap toward achieving this goal. This long-term vision will move biology in a direction that can wield these predictive models for scientific applications that benefit humanity and increase the resilience of natural biological systems. We identify short, medium, and long-term key objectives to connect our current state of knowledge to this long-term vision, iteratively progressing across three stages: (1) utilizing knowledge of biological systems to better inform eco-evolutionary models, (2) generating models with more accurate predictions, and (3) applying predictive models to benefit the biosphere. Within each stage, we outline avenues of investigation and scientific applications related to the timescales over which evolution occurs, the parameter space of eco-evolutionary processes, and the dynamic interactions between these mechanisms. The ability to accurately model, monitor, and anticipate eco-evolutionary changes would be transformational to humanity's interaction with the global environment, providing novel tools to benefit human health, protect the natural world, and manage our planet's biosphere.

Tracking the warriors and spectators of acorn woodpecker wars.

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Wandering woodpeckers: foray behavior in a social bird.

In many cooperatively breeding taxa, nonbreeding subordinates, or helpers, use extra-territorial forays to discover dispersal opportunities. Such forays are considered energetically costly and foraying birds face aggression from conspecific members of the territories they visit. In contrast, breeders in cooperatively breeding taxa are expected to foray seldomly. We used novel tracking technologies to follow 62 acorn woodpeckers (Melanerpes formicivorus), a cooperatively breeding bird, to study extra-territorial foray behavior. Both helpers and breeders engaged in extra-territorial forays routinely and often several times per day. Helpers forayed earlier in the day and invested more time when foraying to high-quality territories. Unexpectedly, breeders forayed as often and as far as helpers. Breeders from high-quality territories forayed closer to their home territories than breeders from low-quality territories, reflecting a potential trade-off between foraying and territory defense. Such a routine pattern of extra-territorial forays in both helpers and breeders suggests that the motives behind forays differ by sex and social status and involve more than simply searching for dispersal opportunities.

Fruiting Season Length Restricts Global Distribution of Female-Only Parental Care in Frugivorous Passerine Birds.

Food availability is known to influence parental care and mating systems in passerine birds. Altricial chicks make uni-parental care particularly demanding for passerines and parental investment is known to increase with decreasing food availability. We expect this to limit uni-parental passerines to habitats with the most consistent food availability. In passerine birds, species having uni-parental care are primarily female-only parental care (female-only care) and most passerine birds with female-only care are frugivores. We predict that frugivorous passerines with female-only care should be restricted to the most stable habitats characterized by longer fruiting season length. At a global scale, female-only care frugivores were distributed in areas with significantly longer fruiting seasons than non-female-only care frugivores. Female-only care species richness had a stronger spatial relationship with longer fruiting season than non-female-only care species richness. Verifying the lack of a phylogenetic signal driving this pattern, our findings indicate that the geographic distribution of female-only care, a geographically and phylogenetically widespread parental care system, is restricted by an extrinsic factor: fruiting season length. This reinstates the importance of food availability on the evolution and maintenance of parental care systems in passerine birds.