Causes and consequences of oxidative stress in a cooperatively breeding bird

Oxidative stress has recently been highlighted as a potential physiological mechanism underpinning life-history trade-offs in animals. While the role of oxidative stress in mediating such trade-offs is receiving increasing attention, its importance in wild populations remains poorly understood. In this thesis, I use a wild population of cooperatively breeding white-browed sparrow weavers (Plocepasser mahali) to investigate the role that oxidative stress plays in mediating the costs of reproduction and immune defence. Cooperative animal societies offer a unique opportunity to investigate the costs of reproduction, because dominants frequently monopolise breeding opportunities (exhibiting higher reproductive effort than subordinates), and subordinate cooperative contributions frequently lighten reproductive workloads. My findings reveal, first, that dominants’ reproductive monopolies do not arise because they exhibit superior oxidative balance, as no such rank-related differences in oxidative state exist prior to breeding (Chapter 2). However, the higher reproductive effort of dominant females may underpin their differential declines in antioxidant protection after the breeding season (Chapter 2). Second, experimental manipulation of reproductive effort reveals marked oxidative damage and body mass costs incurred during reproduction. However, these costs are entirely mitigated in large social groups, suggesting that the cooperative contributions of helpers may offset the costs of reproduction for all group members (Chapter 3). While this represents rare evidence of an oxidative stress cost of reproduction in the wild, longitudinal data suggests that these costs do not endure after the breeding season (Chapter 4), highlighting that circulating markers of oxidative balance are unlikely to mediate long-term costs of reproduction. Finally, an immune activation experiment reveals that, while mounting an immune response causes no net change in oxidative balance, the scale of the response can be adjusted according to baseline antioxidant protection in an oxidative-condition-dependent manner (Chapter 5). Together my results provide support for the role of oxidative stress in shaping life histories in the wild. Furthermore, evidence of rank-related disparities in oxidative balance and the avoidance of reproductive costs in large social groups may have important implications for our understanding of both the evolution of cooperative breeding and the patterns of health and ageing in societies.The research in this thesis was supported by funding from the Natural Environment Research Council (NERC), with additional support from a Biotechnology and Biological Sciences Research Council (BBSRC) David Phillips Research Fellowship and a Royal Society research grant, both held by Dr Andrew J. Young

The oxidative costs of reproduction are group-size dependent in a wild cooperative breeder.

Life-history theory assumes that reproduction entails a cost, and research on cooperatively breeding societies suggests that the cooperative sharing of workloads can reduce this cost. However, the physiological mechanisms that underpin both the costs of reproduction and the benefits of cooperation remain poorly understood. It has been hypothesized that reproductive costs may arise in part from oxidative stress, as reproductive investment may elevate exposure to reactive oxygen species, compromising survival and future reproduction and accelerating senescence. However, experimental evidence of oxidative costs of reproduction in the wild remains scarce. Here, we use a clutch-removal experiment to investigate the oxidative costs of reproduction in a wild cooperatively breeding bird, the white-browed sparrow weaver, Plocepasser mahali. Our results reveal costs of reproduction that are dependent on group size: relative to individuals in groups whose eggs were experimentally removed, individuals in groups that raised offspring experienced an associated cost (elevated oxidative damage and reduced body mass), but only if they were in small groups containing fewer or no helpers. Furthermore, during nestling provisioning, individuals that provisioned at higher rates showed greater within-individual declines in body mass and antioxidant protection. Our results provide rare experimental evidence that reproduction can negatively impact both oxidative status and body mass in the wild, and suggest that these costs can be mitigated in cooperative societies by the presence of additional helpers. These findings have implications for our understanding of the energetic and oxidative costs of reproduction, and the benefits of cooperation in animal societies.This study was funded by a BBSRC David Phillips Fellowship and a Royal Society Research Grant to A.J.Y. and an NERC studentship to D.L.C. J.D.B. was supported by a Royal Society University Research Fellowship.This is the final version of the article. It first appeared from Royal Society Publishing via http://dx.doi.org/10.1098/rspb.2015.203

Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.

Final published versionCopyright: © 2015 Cram et al.The immune system provides vital protection against pathogens, but extensive evidence suggests that mounting immune responses can entail survival and fecundity costs. The physiological mechanisms that underpin these costs remain poorly understood, despite their potentially important role in shaping life-histories. Recent studies involving laboratory models highlight the possibility that oxidative stress could mediate these costs, as immune-activation can increase the production of reactive oxygen species leading to oxidative stress. However, this hypothesis has rarely been tested in free-ranging wild populations, where natural oxidative statuses and compensatory strategies may moderate immune responses and their impacts on oxidative status. Furthermore, the possibility that individuals scale their immune responses according to their oxidative status, conceivably to mitigate such costs, remains virtually unexplored. Here, we experimentally investigate the effects of a phytohaemagglutinin (PHA) immune-challenge on oxidative status in wild male and female white-browed sparrow weavers, Plocepasser mahali. We also establish whether baseline oxidative status prior to challenge predicts the scale of the immune responses. Contrary to previous work on captive animals, our findings suggest that PHA-induced immune-activation does not elicit oxidative stress. Compared with controls (n = 25 birds), PHA-injected birds (n = 27 birds) showed no evidence of a differential change in markers of oxidative damage or enzymatic and non-enzymatic antioxidant protection 24 hours after challenge. We did, however, find that the activity of a key antioxidant enzyme (superoxide dismutase, SOD) prior to immune-activation predicted the scale of the resulting swelling: birds with stronger initial SOD activity subsequently produced smaller swellings. Our findings (i) suggest that wild birds can mount immune responses without suffering from systemic oxidative stress, and (ii) lend support to biomedical evidence that baseline oxidative status can impact the scale of immune responses; a possibility not yet recognised in ecological studies of immunity.Biotechnology and Biological Sciences Research Council (BBSRC)Natural Environment Research Council (NERC)Royal SocietyUniversity of Bristo

Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.

The immune system provides vital protection against pathogens, but extensive evidence suggests that mounting immune responses can entail survival and fecundity costs. The physiological mechanisms that underpin these costs remain poorly understood, despite their potentially important role in shaping life-histories. Recent studies involving laboratory models highlight the possibility that oxidative stress could mediate these costs, as immune-activation can increase the production of reactive oxygen species leading to oxidative stress. However, this hypothesis has rarely been tested in free-ranging wild populations, where natural oxidative statuses and compensatory strategies may moderate immune responses and their impacts on oxidative status. Furthermore, the possibility that individuals scale their immune responses according to their oxidative status, conceivably to mitigate such costs, remains virtually unexplored. Here, we experimentally investigate the effects of a phytohaemagglutinin (PHA) immune-challenge on oxidative status in wild male and female white-browed sparrow weavers, Plocepasser mahali. We also establish whether baseline oxidative status prior to challenge predicts the scale of the immune responses. Contrary to previous work on captive animals, our findings suggest that PHA-induced immune-activation does not elicit oxidative stress. Compared with controls (n = 25 birds), PHA-injected birds (n = 27 birds) showed no evidence of a differential change in markers of oxidative damage or enzymatic and non-enzymatic antioxidant protection 24 hours after challenge. We did, however, find that the activity of a key antioxidant enzyme (superoxide dismutase, SOD) prior to immune-activation predicted the scale of the resulting swelling: birds with stronger initial SOD activity subsequently produced smaller swellings. Our findings (i) suggest that wild birds can mount immune responses without suffering from systemic oxidative stress, and (ii) lend support to biomedical evidence that baseline oxidative status can impact the scale of immune responses; a possibility not yet recognised in ecological studies of immunity

Rank-related contrasts in longevity arise from extra-group excursions not delayed senescence in a cooperative mammal

In many cooperatively breeding animal societies, breeders outlive non-breeding subordinates, despite investing heavily in reproduction [1-3]. In eusocial insects, the extended lifespans of breeders arise from specialized slowed aging profiles [1], prompting suggestions that reproduction and dominance similarly defer aging in cooperatively breeding vertebrates, too [4-6]. Although lacking the permanent castes of eusocial insects, breeders of vertebrate societies could delay aging via phenotypic plasticity (similar rank-related changes occur in growth, neuroendocrinology, and behavior [7-10]), and such plastic deferment of aging may reveal novel targets for preventing aging-related diseases [11]. Here, we investigate whether breeding dominants exhibit extended longevity and delayed age-related physiological declines in wild cooperatively breeding meerkats. We show that dominants outlive subordinates but exhibit faster telomere attrition (a marker of cellular senescence and hallmark of aging [12]) and that in dominants (but not subordinates), rapid telomere attrition is associated with mortality. Our findings further suggest that, rather than resulting from specialized aging profiles, differences in longevity between dominants and subordinates are driven by subordinate dispersal forays, which become exponentially more frequent with age and increase subordinate mortality. These results highlight the need to critically examine the causes of rank-related longevity contrasts in other cooperatively breeding vertebrates, including social mole-rats, where they are currently attributed to specialized aging profiles in dominants [4]

Rank-related contrasts in longevity arise from extra-group excursions not delayed senescence in a cooperative mammal

In many cooperatively breeding animal societies, breeders outlive non-breeding subordinates, despite investing heavily in reproduction [1-3]. In eusocial insects, the extended lifespans of breeders arise from specialized slowed aging profiles [1], prompting suggestions that reproduction and dominance similarly defer aging in cooperatively breeding vertebrates, too [4-6]. Although lacking the permanent castes of eusocial insects, breeders of vertebrate societies could delay aging via phenotypic plasticity (similar rank-related changes occur in growth, neuroendocrinology, and behavior [7-10]), and such plastic deferment of aging may reveal novel targets for preventing aging-related diseases [11]. Here, we investigate whether breeding dominants exhibit extended longevity and delayed age-related physiological declines in wild cooperatively breeding meerkats. We show that dominants outlive subordinates but exhibit faster telomere attrition (a marker of cellular senescence and hallmark of aging [12]) and that in dominants (but not subordinates), rapid telomere attrition is associated with mortality. Our findings further suggest that, rather than resulting from specialized aging profiles, differences in longevity between dominants and subordinates are driven by subordinate dispersal forays, which become exponentially more frequent with age and increase subordinate mortality. These results highlight the need to critically examine the causes of rank-related longevity contrasts in other cooperatively breeding vertebrates, including social mole-rats, where they are currently attributed to specialized aging profiles in dominants [4]

Reproductive conflict resolution in cooperative breeders

Female infanticide is common in animal societies where groups comprise multiple co-breeding females. To reduce the risk that their offspring are killed, mothers can synchronize breeding and pool offspring, making it hard for females to avoid killing their own young. However, female reproductive conflict does not invariably result in reproductive synchrony, and we lack a general hypothesis explaining the variation in conflict resolution strategies seen across species. Here, we investigate the fitness consequences of birth timing relative to other females and the prevalence of birth synchrony in cooperatively breeding Kalahari meerkats (Suricata suricatta). We show that, although there would be substantial benefits to females in synchronizing births and reducing their risk of infanticide, birth synchrony is rare. Since precise breeding synchrony has evolved in a related species with similar infanticidal female reproductive conflict, its absence in meerkats requires an evolutionary explanation. We therefore explore the costs and benefits of synchronizing breeding in two theoretical models, each of which contrasts synchrony with an alternative reproductive strategy: (i) breeding opportunistically and accepting fitness losses to infanticide or (ii) suppressing the reproduction of others to prevent infanticide. Our models show that the costs of synchrony constrain its development if subordinates breed infrequently, and that selection instead favors the suppression of subordinate reproduction by the dominant and opportunistic reproduction by subordinates. Together, our results suggest that the resolution of reproductive conflict in animal societies is shaped by differential breeding propensities among female group members, leading to divergent conflict resolution strategies even in closely related species.A European Research Council grant to T.C.-B. (#294494). A. J. was supported by a Henslow Fellowship jointly provided by the Cambridge Philosophical Society and Hughes Hall, Cambridge. The Kalahari Meerkat Project is supported by the Universities of Cambridge, Zurich and Pretoria.https://academic.oup.com/beheco2020-08-29hj2020Mammal Research InstituteZoology and Entomolog

Reproductive conflict resolution in cooperative breeders

Female infanticide is common in animal societies where groups comprise multiple co-breeding females. To reduce the risk that their offspring are killed, mothers can synchronize breeding and pool offspring, making it hard for females to avoid killing their own young. However, female reproductive conflict does not invariably result in reproductive synchrony, and we lack a general hypothesis explaining the variation in conflict resolution strategies seen across species. Here, we investigate the fitness consequences of birth timing relative to other females and the prevalence of birth synchrony in cooperatively breeding Kalahari meerkats (Suricata suricatta). We show that, although there would be substantial benefits to females in synchronizing births and reducing their risk of infanticide, birth synchrony is rare. Since precise breeding synchrony has evolved in a related species with similar infanticidal female reproductive conflict, its absence in meerkats requires an evolutionary explanation. We therefore explore the costs and benefits of synchronizing breeding in two theoretical models, each of which contrasts synchrony with an alternative reproductive strategy: (i) breeding opportunistically and accepting fitness losses to infanticide or (ii) suppressing the reproduction of others to prevent infanticide. Our models show that the costs of synchrony constrain its development if subordinates breed infrequently, and that selection instead favors the suppression of subordinate reproduction by the dominant and opportunistic reproduction by subordinates. Together, our results suggest that the resolution of reproductive conflict in animal societies is shaped by differential breeding propensities among female group members, leading to divergent conflict resolution strategies even in closely related species.A European Research Council grant to T.C.-B. (#294494). A. J. was supported by a Henslow Fellowship jointly provided by the Cambridge Philosophical Society and Hughes Hall, Cambridge. The Kalahari Meerkat Project is supported by the Universities of Cambridge, Zurich and Pretoria.https://academic.oup.com/beheco2020-08-29hj2020Mammal Research InstituteZoology and Entomolog

Oxidative stress and life histories: unresolved issues and current needs.

Life-history theory concerns the trade-offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life-history trade-offs, but the details remain obscure. As life-history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life-history trade-offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life-history information is available, cannot generally be performed without compromising the aims of the studies that generated the life-history data. There is a need therefore for novel non-invasive measurements of multi-tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life-history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life-history trade-offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life-history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade-offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other

Safeguarding human–wildlife cooperation

Human–wildlife cooperation occurs when humans and free-living wild animals actively coordinate their behavior to achieve a mutually beneficial outcome. These interactions provide important benefits to both the human and wildlife communities involved, have wider impacts on the local ecosystem, and represent a unique intersection of human and animal cultures. The remaining active forms are human–honeyguide and human–dolphin cooperation, but these are at risk of joining several inactive forms (including human–wolf and human–orca cooperation). Human–wildlife cooperation faces a unique set of conservation challenges, as it requires multiple components—a motivated human and wildlife partner, a suitable environment, and compatible interspecies knowledge—which face threats from ecological and cultural changes. To safeguard human–wildlife cooperation, we recommend: (i) establishing ethically sound conservation strategies together with the participating human communities; (ii) conserving opportunities for human and wildlife participation; (iii) protecting suitable environments; (iv) facilitating cultural transmission of traditional knowledge; (v) accessibly archiving Indigenous and scientific knowledge; and (vi) conducting long-term empirical studies to better understand these interactions and identify threats. Tailored safeguarding plans are therefore necessary to protect these diverse and irreplaceable interactions. Broadly, our review highlights that efforts to conserve biological and cultural diversity should carefully consider interactions between human and animal cultures. Please see AfricanHoneyguides.com/abstract-translations for Kiswahili and Portuguese translations of the abstract