Immunogenetic Variation Shapes the Gut Microbiome in a Natural Vertebrate Population

Background: The gut microbiome (GM) can influence many biological processes in the host, impacting its health and survival, but the GM can also be influenced by the host’s traits. In vertebrates, Major Histocompatibility Complex (MHC) genes play a pivotal role in combatting pathogens and are thought to shape the host’s GM. However, despite this - and the documented importance of both GM and MHC variation to individual fitness - few studies have investigated the association between the GM and MHC in the wild. Results: We characterised MHC class I (MHC-I), MHC class II (MHC-II), and GM variation in individuals within a natural population of the Seychelles warbler, Acrocephalus sechellensis. We determined how the diversity and composition of the GM varied with MHC characteristics, in addition to environmental factors and other host intrinsic traits. Our results show that the presence of specific MHC alleles, but not MHC diversity, influences both the diversity and composition of the GM in this population. We found that MHC-I alleles, rather than MHC-II alleles, had the greatest impact on the GM. GM diversity was negatively associated with the presence of three MHC-I alleles (Ase-ua3, Ase-ua4, Ase-ua5), and one MHC-II allele (Ase-dab4), while changes in GM composition were associated with the presence of four different MHC-I alleles (Ase-ua1, Ase-ua7, Ase-ua10, Ase-ua11). GM diversity was also positively correlated with genome-wide heterozygosity and varied with host age and field period.Conclusions: These results suggest that components of the host’s immune system play a role in shaping the GM of wild animals. Host genotype – specifically, adaptive immune receptor MHC-I alleles – can modulate the GM, although whether this occurs directly, or indirectly through effects on host health is unclear. To our knowledge this is the first-time individual MHC-I variation has been shown to be associated with differences in GM characteristics in a natural population. Importantly, it suggests that host–microbiome coevolution may play a role in maintaining functional immunogenetic variation within natural vertebrate populations.

Author Correction: Senescence of song revealed by a long-term study of the Seychelles warbler (Acrocephalus sechellensis)

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Causes and Consequences of Telomere Lengthening in a Wild Vertebrate Population

Telomeres have been advocated to be important markers of biological age in evolutionary and ecological studies. Telomeres usually shorten with age, and shortening is frequently associated with environmental stressors and increased subsequent mortality. Telomere lengthening – an apparent increase in telomere length between repeated samples from the same individual – also occurs. However, the exact circumstances, and consequences, of telomere lengthening are poorly understood. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we tested whether telomere lengthening – which occurs in adults of this species – is associated with specific stressors (reproductive effort, food availability, malarial infection and cooperative breeding) and predicts subsequent survival. In females, telomere shortening was observed under greater stress (i.e. low food availability, malaria infection), while telomere lengthening was observed in females experiencing lower stress (i.e. high food availability, assisted by helpers, without malaria). The telomere dynamics of males were not associated with the key stressors tested. These results indicate that, at least for females, telomere lengthening occurs in circumstances more conducive to self-maintenance. Importantly, both females and males with lengthened telomeres had improved subsequent survival relative to individuals that displayed unchanged, or shortened, telomeres – indicating that telomere lengthening is associated with individual fitness. These results demonstrate that telomere dynamics are bidirectionally responsive to the level of stress that an individual faces, but may poorly reflect the accumulation of stress over the lifetime. This study challenges how we think of telomeres as a marker of biological age.

Senescence of song revealed by a long-term study of the Seychelles warbler (Acrocephalus sechellensis)

Senescence is widespread in nature, often resulting in diminishing survival or reproduction with age, but its role in age-dependent variation in sexual traits is often poorly understood. One reason is that few studies of sexual traits consider non-linear relationships with age, or only consider a narrow range of years relative to the life span of the species. Birdsong has evolved to allow assessment of conspecific quality in numerous bird species. Whilst theory and empirical work suggests that song may become more elaborate with age, there are a paucity of long-term studies testing whether song is associated with age or longevity. In particular, the occurrence of song senescence has rarely been demonstrated. Using an exceptional long-term dataset for the Seychelles warbler (Acrocephalus sechellensis), we analysed relationships between male song, age, survival, and longevity. This species is a long-lived songbird with early life increases, followed by senescent declines, in survival and reproduction. The study population (Cousin Island, Seychelles) is a closed population, with no depredation of adults, providing an excellent opportunity to study senescence in free-living animals. We tested whether song traits were related to age at recording, future survival, longevity, and territory quality. We found age-dependent changes in five song traits (duration, maximum frequency, peak frequency of songs, and duration and frequency bandwidth of trills). Relationships with age were quadratic, indicating reversal in the expression of song coinciding with the onset of senescence in reproduction and survival in this species. One song trait (trill bandwidth) had a quadratic relationship with future survival, but no song traits were related to longevity, suggesting age-related patterns were not the result of selective disappearance. Our study provides one of the first examples of functional senescence in song, offering new insights into avian senescence. Late-life declines in avian song, and possibly other sexual traits, may be more common than currently known, and may play a fundamental role in age-dependent changes in reproductive success.

Telomere heritability and parental age at conception effects in a wild avian population

Individual variation in telomere length is predictive of health and mortality risk across a range of species. However, the relative influence of environmental and genetic variation on individual telomere length in wild populations remains poorly understood. In previous studies, heritability of telomere length has primarily been calculated using parent-offspring regression, but shared environments can confound such estimates. Furthermore, associations with age and parental age at conception effects are typically not accounted for but can also bias heritability estimates. To control for these confounding variables, quantitative genetic ‘animal models’ can be used. However, the few studies on wild populations using this approach have been restricted by power. Here, we investigated the heritability of telomere length and parental age at conception effects in the Seychelles warbler using 2664 telomere length measures from 1318 birds over 20 years and a multi-generational pedigree. We found a weak negative within-paternal age at conception effect (as fathers aged, their offspring had shorter telomeres) and a weak positive between-maternal age at conception effect (females that survived to older ages had offspring with longer telomeres). While parent–offspring regressions did not detect heritability, animal models provided evidence that heritability of telomere length was low in this population. Environmental and technical variation largely influenced telomere length and would have biased heritability estimates if unaccounted for. Estimating the heritability of telomere length is complex, requiring large sample sizes and accounting for confounding effects in order to improve our understanding of the evolutionary potential of telomere length in the wild.

Socio-ecological conditions and female infidelity in the Seychelles warbler

Within socially monogamous breeding systems, levels of extra-pair paternity can vary not only between species, populations, and individuals, but also across time. Uncovering how different extrinsic conditions (ecological, demographic, and social) influence this behavior will help shed light on the factors driving its evolution. Here, we simultaneously address multiple socio-ecological conditions potentially influencing female infidelity in a natural population of the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis. Our contained study population has been monitored for more than 25 years, enabling us to capture variation in socio-ecological conditions between individuals and across time and to accurately assign parentage. We test hypotheses predicting the influence of territory quality, breeding density and synchrony, group size and composition (number and sex of subordinates), and inbreeding avoidance on female infidelity. We find that a larger group size promotes the likelihood of extra-pair paternity in offspring from both dominant and subordinate females, but this paternity is almost always gained by dominant males from outside the group (not by subordinate males within the group). Higher relatedness between a mother and the dominant male in her group also results in more extra-pair paternity—but only for subordinate females—and this does not prevent inbreeding occurring in this population. Our findings highlight the role of social conditions favoring infidelity and contribute toward understanding the evolution of this enigmatic behavior.

Compensatory and additive helper effects in the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis)

ABSTRACTIn cooperatively breeding species, helper aid may affect dominant breeders’ investment trade-offs between current and future reproduction. By compensating for the care provided by helpers, breeders can reduce the costs of reproduction and improve chances of survival. Also, helper care can be additive to that of dominants, resulting in higher success of the current brood.However, the influence of helpers on offspring care itself may be the by-product of group size and territory quality. Therefore to make conclusive inferences about causation of additive and compensatory care as a result of helpper serequires disentangling the impact of helping from other factors determining parental investment.In this study, we use 20 years of offspring provisioning data to investigate the effect of helping on breeder and overall offspring provisioning rates in the facultative cooperatively breeding Seychelles warbler (Acrocephalus sechellensis). Our extensive dataset allowed us to effectively control for the effects of living in a larger group and in territories with higher food availability.We show compensatory and additive care in response to helper aid. Helpers lightened the provisioning load of the dominant male and female and increased the total provisioning to the nestlings. This was irrespective of group size or territory quality (food availability).Our results illustrate how multiple benefits of helping behaviour can simultaneously be fundamental to the evolutionary maintenance of cooperative behaviour.