Adaptation and differentiation across island populations of Berthelot’s pipit (Anthus berthelotii)

The aim of this thesis was to examine how neutral and adaptive processes shape patterns of genetic diversity across populations of Berthelot’s pipit (Anthus berthelotii), a passerine bird endemic to the Canary Islands, Selvagens and Madeira archipelagos. To achieve this, I examined variation in pathogen infection, neutral microsatellites and functional major histocompatibility complex (MHC) genes. I first reviewed previous evidence for pathogen-mediated selection at the MHC, and showed that differentiating between specific mechanisms of balancing selection may not be possible, and that many studies that have attempted to do so have not fully considered alternative explanations. In Berthelot’s pipit, I found marked differences in prevalence of avian malaria and pox across populations, and showed that these differences were stable over time, largely because they were determined by biogeographic features. This, combined with an observed effect on host body condition, suggests that populations face differential selection pressures from pathogens. Microsatellite analyses indicated that the pipit colonised northwards across its range, resulting in genetic bottlenecks in the Selvagens and Madeira archipelagos. I then used the pipit system to assess how population genetic analyses were influenced by microsatellite markers with different levels of variability; lower variability loci appear to more accurately reflect population divergence, whereas higher variability loci better reflect past changes in population size. I also found that two commonly used measures of differentiation (GST and Jost’s D) are both strongly affected by marker variability, but in different ways. Finally, I found that just 11-15 MHC variants persisted through the initial colonisation event. However, since the bottleneck, at least 26 functional MHC alleles have been generated in situ across the different populations, all but two by gene conversion. Taken together, my results provide an interesting example of how founder events, mutation, drift and selection can interact to drive differentiation across natural populations

Spatio-temporal variation in lifelong telomere dynamics in a long-term ecological study

1. Understanding individual-level variation in response to the environment is fundamental to understanding life-history evolution and population dynamics. Telomeres, the protective caps at the ends of chromosomes, shorten in response to oxidative stress, and telomere shortening is correlated with reduced survival and lifespan. Investigating telomere dynamics may help us quantify individual variation in the costs experienced from social and ecological factors, and enhance our understanding of the dynamics of natural populations. 2. Here we study spatio-temporal variation in lifelong telomere dynamics in the Seychelles warbler, Acrocephalus sechellensis. We combine long-term life-history and ecological data with a large longitudinal dataset of mean telomere lengths, consisting of 1808 samples from 22 cohorts born between 1993 and 2014. We provide a detailed analysis of how telomere dynamics vary over individual lifespans and cohorts, and with spatio-temporal variation in the social and ecological environment. 3. We found that telomere length decreases with cross-sectional and longitudinal measures of age, and most rapidly very early in life. However, both cross-sectional and longitudinal data suggested that against this overall pattern of shortening, bouts of telomere length increase occur in some individuals. Using a large number of repeated measurements we show statistically that these increases are unlikely to be explained solely by qPCR measurement error. 4. Telomere length varied markedly among cohorts. Telomere length was positively associated with temporal variation in island-wide insect abundance - a key resource for the insectivorous Seychelles warbler - suggesting that the costs associated with living in harsher environments can be studied by investigating telomere dynamics. We also found evidence for sex-specific relationships between telomeres and tarsus length, potentially reflecting differential costs of growth. 5. Our long-term data show that in a natural population, telomere dynamics vary in a complex manner over individual lifespans, and across space and time. Variance in telomere dynamics among individuals is the product of a wide array of genetic, parental and environmental factors. Explaining this variation more fully will require the integration of comprehensive long-term ecological and genetic data from multiple populations and species

Breeders that receive help age more slowly in a cooperatively breeding bird.

Helping by group members is predicted to lead to delayed senescence by affecting the trade-off between current reproduction and future survival for dominant breeders. Here we investigate this prediction in the Seychelles warbler, Acrocephalus sechellensis, in which mainly female subordinate helpers (both co-breeders and non-breeding helpers) often help dominants raise offspring. We find that the late-life decline in survival usually observed in this species is greatly reduced in female dominants when a helper is present. Female dominants with a female helper show reduced telomere attrition, a measure that reflects biological ageing in this and other species. Finally, the probability of having female, but not male, helpers increases with dominant female age. Our results suggest that delayed senescence is a key benefit of cooperative breeding for elderly dominants and support the idea that sociality and delayed senescence are positively self-reinforcing. Such an effect may help explain why social species often have longer lifespans

Heritability of telomere variation: it’s all about the environment!

Individual differences in telomere length have been linked to survival and ageing. Understanding the heritability of telomere length can provide important insight into individual differences and facilitate our understanding of the evolution of telomeres. However to gain accurate and meaningful estimates of telomere heritability it is vital that the impact of the environment, and how thismay vary, is understood and accounted for. The aim of this review is to raise awareness of this important, but much under-appreciated point.We outline the factors known to impact telomere length and discuss the fact that telomere length is a trait that changes with age. We highlight statistical methods that can separate genetic from environmental effects and control for confounding variables. We then reviewhowwell previous studies in natural vertebrate populations have taken these factors into account. We argue that studies to date either use methodological techniques that confound environmental and genetic effects, or use appropriate methods but lack sufficient power to fully separate these components.We discuss potential solutions.We conclude that we need larger studies, which also span longer time periods, to account for changing environmental effects, if we are to determine meaningful estimates of the genetic component of telomere length. This article is part of the theme issue ‘Understanding diversity in telomere dynamics'

Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations

The genes of the major histocompatibility complex are the most polymorphic genes in vertebrates, with more than 1,000 alleles described in human populations. How this polymorphism is maintained, however, remains an evolutionary puzzle. Major histocompatibility complex genes have a crucial function in the adaptive immune system by presenting parasite-derived antigens to T lymphocytes. Because of this function, varying parasite-mediated selection has been proposed as a major evolutionary force for maintaining major histocompatibility complex polymorphism. A necessary prerequisite of such a balancing selection process is rapid major histocompatibility complex allele frequency shifts resulting from emerging selection by a specific parasite. Here we show in six experimental populations of sticklebacks, each exposed to one of two different parasites, that only those major histocompatibility complex alleles providing resistance to the respective specific parasite increased in frequency in the next host generation. This result demonstrates experimentally that varying parasite selection causes rapid adaptive evolutionary changes, thus facilitating the maintenance of major histocompatibility complex polymorphism

Evolutionary genetics of immunological supertypes reveals two faces of the Red Queen

Red Queen host-parasite co-evolution can drive adaptations of immune-genes by positive selection that erodes genetic variation (Red Queen Arms Race), or result in a balanced polymorphism (Red Queen Dynamics) and the long-term preservation of genetic variation (trans-species polymorphism). These two Red Queen processes are opposite extremes of the co-evolutionary spectrum. Here we show that both Red Queen processes can operate simultaneously, analyzing the Major Histocompatibility Complex (MHC) in guppies (Poecilia reticulata and P. obscura), and swamp guppies (Micropoecilia picta). Sub-functionalization of MHC alleles into “supertypes” explains how polymorphisms persist during rapid host-parasite co-evolution. Simulations show the maintenance of supertypes as balanced polymorphisms, consistent with Red Queen Dynamics, whereas alleles within supertypes are subject to positive selection in a Red Queen Arms Race. Building on the Divergent Allele Advantage hypothesis, we show that functional aspects of allelic diversity help to elucidate the evolution of polymorphic genes involved in Red Queen co-evolution

High major histocompatibility complex class I polymorphism despite bottlenecks in wild and domesticated populations of the zebra finch ()

Background Two subspecies of zebra finch, Taeniopygia guttata castanotis and T. g. guttata are native to Australia and the Lesser Sunda Islands, respectively. The Australian subspecies has been domesticated and is now an important model system for research. Both the Lesser Sundan subspecies and domesticated Australian zebra finches have undergone population bottlenecks in their history, and previous analyses using neutral markers have reported reduced neutral genetic diversity in these populations. Here we characterize patterns of variation in the third exon of the highly variable major histocompatibility complex (MHC) class I α chain. As a benchmark for neutral divergence, we also report the first mitochondrial NADH dehydrogenase 2 (ND2) sequences in this important model system. Results Despite natural and human-mediated population bottlenecks, we find that high MHC class I polymorphism persists across all populations. As expected, we find higher levels of nucleotide diversity in the MHC locus relative to neutral loci, and strong evidence of positive selection acting on important residues forming the peptide-binding region (PBR). Clear population differentiation of MHC allele frequencies is also evident, and this may be due to adaptation to new habitats and associated pathogens and/or genetic drift. Whereas the MHC Class I locus shows broad haplotype sharing across populations, ND2 is the first locus surveyed to date to show reciprocal monophyly of the two subspecies. Conclusions Despite genetic bottlenecks and genetic drift, all surveyed zebra finch populations have maintained high MHC Class I diversity. The diversity at the MHC Class I locus in the Lesser Sundan subspecies contrasts sharply with the lack of diversity in previously examined neutral loci, and may thus be a result of selection acting to maintain polymorphism. Given uncertainty in historical population demography, however, it is difficult to rule out neutral processes in maintaining the observed diversity. The surveyed populations also differ in MHC Class I allele frequencies, and future studies are needed to assess whether these changes result in functional immune differences

Evolutionary Determinants of Genetic Variation in Susceptibility to Infectious Diseases in Humans

Although genetic variation among humans in their susceptibility to infectious diseases has long been appreciated, little focus has been devoted to identifying patterns in levels of variation in susceptibility to different diseases. Levels of genetic variation in susceptibility associated with 40 human infectious diseases were assessed by a survey of studies on both pedigree-based quantitative variation, as well as studies on different classes of marker alleles. These estimates were correlated with pathogen traits, epidemiological characteristics, and effectiveness of the human immune response. The strongest predictors of levels of genetic variation in susceptibility were disease characteristics negatively associated with immune effectiveness. High levels of genetic variation were associated with diseases with long infectious periods and for which vaccine development attempts have been unsuccessful. These findings are consistent with predictions based on theoretical models incorporating fitness costs associated with the different types of resistance mechanisms. An appreciation of these observed patterns will be a valuable tool in directing future research given that genetic variation in disease susceptibility has large implications for vaccine development and epidemiology

Temporal and spatial instability in neutral and adaptive (MHC) genetic variation in marginal salmon populations

The role of marginal populations for the long-term maintenance of species’ genetic diversity and evolutionary potential is particularly timely in view of the range shifts caused by climate change. The Centre-Periphery hypothesis predicts that marginal populations should bear reduced genetic diversity and have low evolutionary potential. We analysed temporal stability at neutral microsatellite and adaptive MHC genetic variation over five decades in four marginal Atlantic salmon populations located at the southern limit of the species’ distribution with a complicated demographic history, which includes stocking with foreign and native salmon for at least 2 decades. We found a temporal increase in neutral genetic variation, as well as temporal instability in population structuring, highlighting the importance of temporal analyses in studies that examine the genetic diversity of peripheral populations at the margins of the species’ range, particularly in face of climate change