Accounting for heteroscedasticity and censoring in chromosome partitioning analyses

A fundamental assumption in quantitative genetics is that traits are controlled by many loci of small effect. Using genomic data, this assumption can be tested using chromosome partitioning analyses, where the proportion of genetic variance for a trait explained by each chromosome (h(c)(2)), is regressed on its size. However, as h(c)(2)-estimates are necessarily positive (censoring) and the variance increases with chromosome size (heteroscedasticity), two fundamental assumptions of ordinary least squares (OLS) regression are violated. Using simulated and empirical data we demonstrate that these violations lead to incorrect inference of genetic architecture. The degree of bias depends mainly on the number of chromosomes and their size distribution and is therefore specific to the species; using published data across many different species we estimate that not accounting for this effect overall resulted in 28% false positives. We introduce a new and computationally efficient resampling method that corrects for inflation caused by heteroscedasticity and censoring and that works under a large range of dataset sizes and genetic architectures in empirical datasets. Our new method substantially improves the robustness of inferences from chromosome partitioning analyses.Peer reviewe

Ecological genetics of populations experiencing changing environmental conditions

A major goal in evolutionary biology is to understand how ecological factors shape the phenotypic and genetic variation that we observe in natural populations and in this thesis I examine how rapid changes in temperature have influenced phenotypic and genetic variation in morphological and life history traits in long-term studies of great tits. In Chapter 1 I review what is known about the effects of environmental change on natural populations, and outline the quantitative genetic framework that is available to study genetic variation in natural populations. Much focus on the effects of climate change has concerned species’ phenology, far less attention has been given to other traits. In Chapter 2 I examine the effects changing environmental conditions have had on the proportion of females that produce second broods. Temperature operates mainly through indirect effects (such as food abundance) but may also have more direct effects. In Chapter 3 I show that over a 36 year period body size have declined in line with predictions from Bergmann’s rule and I explore the genetic basis of this decline and the environmental factors involved. Although we can learn much from population level responses, there is a great deal of additional information to be gained by studying between-individual responses. In Chapter 4 I therefore compare the multivariate pattern of between-individual variation in phenotypic plasticity and its genetic basis for laying date and clutch size, in two great tit populations. Environmental changes may also directly affect the expression of genetic variance as well as the strength of selection acting on a trait, and in Chapter 5 I show that, for laying date, the environment induces a positive covariance between strength of selection and the expression of additive genetic variance, something that may enhance the rate of adaptation. Finally, in Chapter 6 I discuss and summarise the wider implications of the findings from this thesis

Effects of environment and genotype on dispersal differ across departure, transfer and settlement in a butterfly metapopulation

Active dispersal is driven by extrinsic and intrinsic factors at the three stages of departure, transfer and settlement. Most empirical studies capture only one stage of this complex process, and knowledge of how much can be generalized from one stage to another remains unknown. Here we use genetic assignment tests to reconstruct dispersal across 5 years and 232 habitat patches of a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We link individual dispersal events to weather, landscape structure, size and quality of habitat patches, and individual genotype to identify the factors that influence the three stages of dispersal and post-settlement survival. We found that nearly all tested factors strongly affected departure probabilities, but that the same factors explained very little variation in realized dispersal distances. Surprisingly, we found no effect of dispersal distance on post-settlement survival. Rather, survival was influenced by weather conditions, quality of the natal habitat patch, and a strong interaction between genotype and occupancy status of the settled habitat patch, with more mobile genotypes having higher survival as colonists rather than as immigrants. Our work highlights the multi-causality of dispersal and that some dispersal costs can only be understood by considering extrinsic and intrinsic factors and their interaction across the entire dispersal process.Peer reviewe

Patterns of Cryptic Diversity and Phylogeography in Four Freshwater Copepod Crustaceans in European Lakes

Comparative phylogeography has become a powerful approach in exploring hidden or cryptic diversity within widespread species and understanding how historical and biogeographical factors shape the modern patterns of their distribution. Most comparative phylogeographic studies so far focus on terrestrial and vertebrate taxa, while aquatic invertebrates (and especially freshwater invertebrates) remain unstudied. In this article, we explore and compare the patterns of molecular diversity and phylogeographic structure of four widespread freshwater copepod crustaceans in European water bodies: the harpacticoids Attheyella crassa, Canthocamptus staphylinus and Nitokra hibernica, and the cyclopoid Eucyclops serrulatus, using sequence data from mtDNA COI and nuclear ITS/18S rRNA genes. The three taxa A. crassa, C. staphylinus and E. serrulatus each consist of deeply diverged clusters and are deemed to represent complexes of species with largely (but not completely) non-overlapping distributions, while in N. hibernica only little differentiation was found, which may however reflect the geographically more restricted sampling. However, the geographical patterns of subdivision differ. The divisions in A. crassa and E. serrulatus follow an east–west pattern in Northern Europe whereas that in C. staphylinus has more of a north–south pattern, with a distinct Fennoscandian clade. The deep mitochondrial splits among populations of A. crassa, C. staphylinus and E. serrulatus (model-corrected distances 26–36%) suggest that divergence of the lineages predate the Pleistocene glaciations. This study provides an insight into cryptic diversity and biogeographic distribution of freshwater copepods

Patterns of Cryptic Diversity and Phylogeography in Four Freshwater Copepod Crustaceans in European Lakes

Comparative phylogeography has become a powerful approach in exploring hidden or cryptic diversity within widespread species and understanding how historical and biogeographical factors shape the modern patterns of their distribution. Most comparative phylogeographic studies so far focus on terrestrial and vertebrate taxa, while aquatic invertebrates (and especially freshwater invertebrates) remain unstudied. In this article, we explore and compare the patterns of molecular diversity and phylogeographic structure of four widespread freshwater copepod crustaceans in European water bodies: the harpacticoids Attheyella crassa, Canthocamptus staphylinus and Nitokra hibernica, and the cyclopoid Eucyclops serrulatus, using sequence data from mtDNA COI and nuclear ITS/18S rRNA genes. The three taxa A. crassa, C. staphylinus and E. serrulatus each consist of deeply diverged clusters and are deemed to represent complexes of species with largely (but not completely) non-overlapping distributions, while in N. hibernica only little differentiation was found, which may however reflect the geographically more restricted sampling. However, the geographical patterns of subdivision differ. The divisions in A. crassa and E. serrulatus follow an east–west pattern in Northern Europe whereas that in C. staphylinus has more of a north–south pattern, with a distinct Fennoscandian clade. The deep mitochondrial splits among populations of A. crassa, C. staphylinus and E. serrulatus (model-corrected distances 26–36%) suggest that divergence of the lineages predate the Pleistocene glaciations. This study provides an insight into cryptic diversity and biogeographic distribution of freshwater copepods

Assortative mating in an ecological context:Effects of mate choice errors and relative species abundance on the frequency and asymmetry of hybridization

The frequency and asymmetry of mixed-species mating set the initial stage for the ecological and evolutionary implications of hybridization. How such patterns of mixed-species mating, in turn, are influenced by the combination of mate choice errors and relative species abundance remains largely unknown. We develop a mathematical model that generates predictions for how relative species abundances and mate choice errors affect hybridization patterns. When mate choice errors are small (5%), the highest hybridization frequency occurs when species occur in equal proportions. Furthermore, females of the less abundant species are overrepresented in mixed-species matings. We compare our theoretical predictions with empirical data on naturally hybridizing Ficedula flycatchers and find that hybridization is highest when the two species occur in equal abundance, implying rather high mate choice errors. We discuss ecological and evolutionary implications of our findings and encourage future work on hybrid zone dynamics that take demographic aspects, such as relative species abundance, into account

Quantitative genetic analysis of brain size variation in sticklebacks: support for the mosaic model of brain evolution

The mosaic model of brain evolution postulates that different brain regions are relatively free to evolve independently from each other. Such independent evolution is possible only if genetic correlations among the different brain regions are less than unity. We estimated heritabilities, evolvabilities and genetic correlations of relative size of the brain, and its different regions in the three-spined stickleback (Gasterosteus aculeatus). We found that heritabilities were low (average h2 = 0.24), suggesting a large plastic component to brain architecture. However, evolvabilities of different brain parts were moderate, suggesting the presence of additive genetic variance to sustain a response to selection in the long term. Genetic correlations among different brain regions were low (average rG = 0.40) and significantly less than unity. These results, along with those from analyses of phenotypic and genetic integration, indicate a high degree of independence between different brain regions, suggesting that responses to selection are unlikely to be severely constrained by genetic and phenotypic correlations. Hence, the results give strong support for the mosaic model of brain evolution. However, the genetic correlation between brain and body size was high (rG = 0.89), suggesting a constraint for independent evolution of brain and body size in sticklebacks

Comparative support for the expensive tissue hypothesis: big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids.

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and i) investment into other costly tissues, ii) overall metabolic rate, and iii) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large-scale patterns of brain size evolution also in ectothermic vertebrates. Here we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates. This article is protected by copyright. All rights reserved.Peer reviewe

Rapid changes in DNA methylation associated with the initiation of reproduction in a small songbird

Species with a circannual life cycle need to match the timing of their life history events to the environment to maximize fitness. However, our understanding of how circannual traits such as timing of reproduction are regulated on a molecular level remains limited. Recent studies have implicated that epigenetic mechanisms can be an important part in the processes that regulate circannual traits. Here, we explore the role of DNA methylation in mediating reproductive timing in a seasonally breeding bird species, the great tit (Parus major), using genome-wide DNA methylation data from individual females that were blood sampled repeatedly throughout the breeding season. We demonstrate rapid and directional changes in DNA methylation within the promoter region of several genes, including a key transcription factor (NR5A1) known from earlier studies to be involved in the initiation of timing of reproduction. Interestingly, the observed changes in DNA methylation at NR5A1 identified here are in line with earlier gene expression studies of reproduction in chicken, indicating that the observed shifts in DNA methylation at this gene can have a regulatory role. Our findings provide an important step towards elucidating the genomic mechanism that mediates seasonal timing of a key life history traits and provide support for the idea that epigenetic mechanisms may play an important role in circannual traits.Peer reviewe

Social networks strongly predict the gut microbiota of wild mice

The mammalian gut teems with microbes, yet how hosts acquire these symbionts remains poorly understood. Research in primates suggests that microbes can be picked up via social contact, but the role of social interactions in non-group-living species remains underexplored. Here, we use a passive tracking system to collect high resolution spatiotemporal activity data from wild mice (Apodemus sylvaticus). Social network analysis revealed social association strength to be the strongest predictor of microbiota similarity among individuals, controlling for factors including spatial proximity and kinship, which had far smaller or nonsignificant effects. This social effect was limited to interactions involving males (male-male and male-female), implicating sex-dependent behaviours as driving processes. Social network position also predicted microbiota richness, with well-connected individuals having the most diverse microbiotas. Overall, these findings suggest social contact provides a key transmission pathway for gut symbionts even in relatively asocial mammals, that strongly shapes the adult gut microbiota. This work underlines the potential for individuals to pick up beneficial symbionts as well as pathogens from social interactions.Peer reviewe