Early-life conditions impact juvenile telomere length, but do not predict later life-history strategies or fitness in a wild vertebrate.

Environmental conditions experienced during early life may have long-lasting effects on later-life phenotypes and fitness. Individuals experiencing poor early-life conditions may suffer subsequent fitness constraints. Alternatively, individuals may use a strategic "Predictive Adaptive Response" (PAR), whereby they respond-in terms of physiology or life-history strategy-to the conditions experienced in early life to maximize later-life fitness. Particularly, the Future Lifespan Expectation (FLE) PAR hypothesis predicts that when poor early-life conditions negatively impact an individual's physiological state, it will accelerate its reproductive schedule to maximize fitness during its shorter predicted life span. We aimed to measure the impact of early-life conditions and resulting fitness across individual lifetimes to test predictions of the FLE hypothesis in a wild, long-lived model species. Using a long-term individual-based dataset, we investigated how early-life conditions are linked with subsequent fitness in an isolated population of the Seychelles warbler Acrocephalus sechellensis. How individuals experience early-life environmental conditions may vary greatly, so we also tested whether telomere length-shorter telomers are a biomarker of an individual's exposure to stress-can provide an effective measure of the individual-specific impact of early-life conditions. Specifically, under the FLE hypothesis, we would expect shorter telomeres to be associated with accelerated reproduction. Contrary to expectations, shorter juvenile telomere length was not associated with poor early-life conditions, but instead with better conditions, probably as a result of faster juvenile growth. Furthermore, neither juvenile telomere length, nor other measures of early-life conditions, were associated with age of first reproduction or the number of offspring produced during early life in either sex. We found no support for the FLE hypothesis. However, for males, poor early-life body condition was associated with lower first-year survival and reduced longevity, indicating that poor early-life conditions pose subsequent fitness constraints. Our results also showed that using juvenile telomere length as a measure of early-life conditions requires caution, as it is likely to not only reflect environmental stress but also other processes such as growth.

Correction: Rapid loss of flight in the Aldabra white-throated rail.

[This corrects the article DOI: 10.1371/journal.pone.0226064.].

Rapid loss of flight in the Aldabra white-throated rail.

Flight loss has evolved independently in numerous island bird lineages worldwide, and particularly in rails (Rallidae). The Aldabra white-throated rail (Dryolimnas [cuvieri] aldabranus) is the last surviving flightless bird in the western Indian Ocean, and the only living flightless subspecies within Dryolimnas cuvieri, which is otherwise volant across its extant range. Such a difference in flight capacity among populations of a single species is unusual, and could be due to rapid evolution of flight loss, or greater evolutionary divergence than can readily be detected by traditional taxonomic approaches. Here we used genetic and morphological analyses to investigate evolutionary trajectories of living and extinct Dryolimnas cuvieri subspecies. Our data places D. [c.] aldabranus among the most rapid documented avian flight loss cases (within an estimated maximum of 80,000-130,000 years). However, the unusual intraspecific variability in flight capacity within D. cuvieri is best explained by levels of genetic divergence, which exceed those documented between other volant taxa versus flightless close relatives, all of which have full species status. Our results also support consideration of Dryolimnas [cuvieri] aldabranus as sufficiently evolutionary distinct from D. c. cuvieri to warrant management as an evolutionary significant unit. Trait variability among closely related lineages should be considered when assessing conservation status, particularly for traits known to influence vulnerability to extinction (e.g. flightlessness).

Senescence in the wild: Insights from a long-term study on Seychelles warblers.

Senescence--the progressive age-dependent decline in performance--occurs in most organisms. There is considerable variation in the onset and rate of senescence between and within species. Yet the causes of this variation are still poorly understood, despite being central to understanding the evolution of senescence. Long-term longitudinal studies on wild animals are extremely well-suited to studying the impact of environmental and individual characteristics (and the interaction between the two) on senescence, and can help us to understand the mechanisms that shape the evolution of senescence. In this review, we summarize and discuss the insights gained from our comprehensive long-term individual-based study of the Seychelles warbler (Acrocephalus sechellensis). This species provides an excellent model system in which to investigate the evolution of senescence in the wild. We found that Seychelles warblers show senescent declines in survival and reproduction, and discuss how individual characteristics (body condition, body size) and environmental effects (low- versus high-quality environments) may affect the onset and rate of senescence. Further, we highlight the evidence for trade-offs between early-life investment and senescence. We describe how key cellular and physiological processes (oxidative stress and telomere shortening) underpinning senescence are affected by individual and environmental characteristics in the Seychelles warbler (e.g. food availability, reproductive investment, disease) and we discuss how such physiological variation may mediate the relationship between environmental characteristics and senescence. Based on our work using Seychelles warblers as a model system, we show how insights from long-term studies of wild animals may help unravel the causes of the remarkable variation in senescence observed in natural systems, and highlight areas for promising future research.

Persistence of distinctive morphotypes in the native range of the CITES-listed Aldabra giant tortoise.

Understanding the extent of morphological variation in the wild population of Aldabra giant tortoises is important for conservation, as morphological variation in captive populations has been interpreted as evidence for lingering genes from extinct tortoise lineages. If true, this could impact reintroduction programmes in the region. The population of giant tortoises on Aldabra Atoll is subdivided and distributed around several islands. Although pronounced morphological variation was recorded in the late 1960s, it was thought to be a temporary phenomenon. Early researchers also raised concerns over the future of the population, which was perceived to have exceeded its carrying capacity. We analyzed monthly monitoring data from 12 transects spanning a recent 15-year period (1998-2012) during which animals from four subpopulations were counted, measured, and sexed. In addition, we analyzed survival data from individuals first tagged during the early 1970s. The population is stable with no sign of significant decline. Subpopulations differ in density, but these differences are mostly due to differences in the prevailing vegetation type. However, subpopulations differ greatly in both the size of animals and the degree of sexual dimorphism. Comparisons with historical data reveal that phenotypic differences among the subpopulations of tortoises on Aldabra have been apparent for the last 50 years with no sign of diminishing. We conclude that the giant tortoise population on Aldabra is subject to varying ecological selection pressures, giving rise to stable morphotypes in discrete subpopulations. We suggest therefore that (1) the presence of morphological differences among captive Aldabra tortoises does not alone provide convincing evidence of genes from other extinct species; and (2) Aldabra serves as an important example of how conservation and management in situ can add to the scientific value of populations and perhaps enable them to better adapt to future ecological pressures.

Parasitic infection and oxidative status are associated and vary with breeding activity in the Seychelles warbler.

Parasites can have detrimental effects on host fitness, and infection typically results in the stimulation of the immune system. While defending against infection, the immune system generates toxic oxidants; if these are not sufficiently counteracted by the antioxidant system, a state of oxidative stress can occur. Here, we investigated the relationship between parasitic infection-using malarial infection as a model-and oxidative status in a natural population of the Seychelles warbler, while taking into account potentially interacting environmental covariates. We found that malaria is associated with increased susceptibility to oxidative stress, but this depends on the breeding stage: only during the energetically demanding provisioning stage did infected birds have higher oxidative stress susceptibility than non-infected birds. The imbalance in oxidative status was caused by a marked increase in oxidant levels observed only in infected birds during provisioning and by an overall reduction in antioxidant capacity observed in all birds across the breeding cycle. This finding implies that higher workload while dealing with an infection could aggravate oxidative repercussions. Malarial infection was not associated with body condition loss, suggesting that even when conditional effects are not directly visible, detrimental effects may still manifest themselves over the longer term through the oxidative consequences.

Assessing the cost of helping: the roles of body condition and oxidative balance in the Seychelles warbler (Acrocephalus sechellensis).

In cooperatively breeding species, helping close relatives may provide important fitness benefits. However, helping can be energetically expensive and may result in increased generation of reactive oxygen species. Consequently, an oxidant/antioxidant imbalance can lead to higher oxidative stress susceptibility. Given the potential costs of helping, it may be that only individuals with a sufficiently good body condition and/or stable oxidative balance can afford to help. Knowledge about relationships between social status and oxidative balance in cooperatively breeding systems is still limited. Studying these relationships is important for understanding the costs of helping and physiological pressures of reproduction. Here we evaluate the relationship between helping behaviour, body condition and oxidative balance in a wild population of the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis). In this species, some subordinate individuals help dominant birds with the rearing of young, while others refrain from any assistance. We assessed body condition and oxidative parameters of birds of different social status caught during different breeding stages. We found that, prior to breeding, female subordinates that did not subsequently help (non-helpers) had significantly lower body condition and higher ROMs (reactive oxygen metabolites) than helpers and dominants. During the later stages of breeding, body condition was low in dominants and helpers, but high in non-helpers. Differences in oxidative balance between individuals of different social status were found only during nest care: Dominant males occupied with guarding behaviours tended to have relatively high oxidative stress susceptibility. Furthermore, dominant and helper females showed elevated antioxidant capacity (measured as OXY) in the weeks just prior to egg-laying, possibly representing a change in their reproductive physiology. The results imply that an individuals' oxidative balance may be influenced by factors related to reproduction, which can differ with sex and--within cooperative breeding systems--social status.

Spatio-temporal variation in territory quality and oxidative status: a natural experiment in the Seychelles warbler (Acrocephalus sechellensis).

1. Fluctuations in the quality of the habitat in which an animal lives can have major consequences for its behaviour and physiological state. In poor-quality habitat with low food availability, metabolically intensive foraging activity is likely to result in increased generation of reactive oxygen species, while scarcity of food can lead to a weakening of exogenously derived antioxidant defences. The consequent oxidant/antioxidant imbalance may lead to elevated oxidative stress. 2. Although the link between food availability and oxidative stress has been studied in the laboratory, very little is known about this relationship in the wild. Here, we investigate the association between territory quality (measured through food availability) and oxidative stress in the Seychelles warbler (Acrocephalus sechellensis). 3. Seychelles warblers are insectivorous birds that inhabit a fixed feeding territory year round. Individuals experience profound and rapid local fluctuations in territory quality within these territories, owing to changing patterns of vegetation defoliation resulting from seasonal changes in prevailing wind direction and wind-borne salt spray. 4. As expected, oxidant generation (measured as reactive oxygen metabolites; ROMs) was higher when territory quality was low, but there was no correlation between territory quality and antioxidant capacity (OXY). The negative correlation between territory quality and ROMs was significant between individuals and approached significance within individuals, indicating that the pattern resulted from individual responses to environmental variation. 5. ROMs and OXY levels within individuals were positively correlated, but the relationship between territory quality and ROMs persisted after including OXY as a covariate, implying that oxidative stress occurs in low territory quality conditions. 6. Our results indicate that the oxidative stress balance of an individual is sensitive to relatively short-term changes in territory quality, which may have consequences for the birds' fitness.

Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: implications for ecologists.

One route to gain insight into the causes and consequences of ecological differentiation is to understand the underlying physiological mechanisms. We explored the relationships between immunological and oxidative status and investigated how birds cope physiologically with the effects of immune-derived oxidative damage. We successively implemented two experimental manipulations to alter physiological status in a model bird species: the homing pigeon (Columba livia). The first manipulation, an immune supplementation, was achieved by oral administration of lysozyme, a naturally occurring and non-specific antimicrobial enzyme. The second manipulation, an immune challenge, took the form of an injection with lipopolysaccharide, a bacterial endotoxin. Between groups of lysozyme-treated and control birds, we compared lipopolysaccharide-induced changes in reactive oxygen metabolites, total antioxidant capacity, haptoglobin, oxygen consumption, body mass and cloacal temperature. Lysozyme supplementation intensified the lipopolysaccharide-induced inflammatory response and generated short-term oxidative and metabolic costs. We identified significant interactions between immune supplementation and immune challenge in terms of reactive oxygen metabolites, haptoglobin and oxygen consumption. Our study provides alternative interpretations of differences in oxidative and immunological indices and demonstrates that these indices can also fluctuate and interact across very short time scales, reflecting something akin to current 'health status' or 'physiological condition'. These ephemeral effects highlight the need to broadly consider current physiological condition when drawing conclusions that relate physiology to ecology and evolution.

Testosterone, cuckoldry risk and extra-pair opportunities in the Seychelles warbler.

In male birds, testosterone (T) plays an important role in aggressive and mate-attraction behaviour. In the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis, extra-group copulations (EGCs) occur frequently, but are not accompanied by sexual courtship displays as in within-pair copulations. Paternity is nearly always gained by primary males. We investigated whether T levels and sperm storage capability (cloacal protuberance (CP)) in adult primary and subordinate males were related to timing of egg laying, levels of cuckoldry and extra-group paternity (EGP) opportunities. During the sexually active period before egg laying, T levels and CP were only elevated or enlarged (respectively) in primary males, and some suggestion was found that subordinate males do not invest in elevated T levels. The peak in T occurred during the fertile period of the female partner and corresponded to the peak period of male sexual displays and mate guarding, but was independent of cuckoldry risk (density of neighbouring primary males). CP was also enhanced during this period; however, CP but not T remained elevated after egg laying by their mates, and CP but not T was positively related to EGP opportunities (density of neighbouring fertile females). We conclude that T is involved in sexual courtship displays and mate guarding, but not in gaining EGCs. These findings contrast with those in other species where EGP involves elaborate sexual displays.