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Author
Date
2021Type
- Doctoral Thesis
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Abstract
The fundamental evolutionary forces of drift, gene flow, selection and mutation are at constant play in natural populations; acting and interacting under the constraints and contexts of populations’ prevailing environment as well as demographic history. As environments change - and populations migrate, change in size or adapt in response - these evolutionary forces leave distinct signatures in the patterns of neutral and adaptive genetic variation in populations. We can infer much about the history of populations and species, and of evolutionary processes, from unravelling these patterns. However, this can be challenging to accomplish when the population or species’ demographic history is complex, as under such scenarios, neutral processes (i.e. drift and migration) can generate similar and hence confounding patterns to adaptive processes. In this thesis, I evaluate how we can disentangle such patterns to identify genetic loci under selection (Chapter I) and evaluate how neutral and adaptive processes can interact under complex demography and fluctuating environments to give rise to the patterns of genetic variation we observe in natural populations today (Chapter II and Chapter III).
In Chapter I, we derive a methodological framework to infer loci under selection given arbitrarily complex demographies. In our newly developed method which we name ‘LSD’ (identifying Loci under Selection under explicit Demographic models), we employ coalescent modelling under an approximate Bayesian computation (ABC) framework to estimate demographic parameters in a sliding window across the genome and identify windows that are significantly divergent from the neutral, or genome-wide, expectations - under the premise that selection generates deviations in demographic parameters (i.e. drift and migration) away from genome-wide expectations. We show, via simulations and a case study, that our approach has several advantages. First, as the method is based on user-defined, explicit demographic models, demographic history is accounted for explicitly. This allows it to outperform current genome-scan methods under complex demographies. Second, the method can simultaneously incorporate information from many different, complementary summary statistics. Third, under multi-population systems, the method can accurately infer in which specific population selection acts, and thus characterise genetic trade-offs directly from genetic data. Finally, the method is highly customisable and can potentially be applied to detect various forms of selection including positive, divergent and balancing selection, in addition to adaptive introgression.
In Chapter II, we focus our attention on the genetic legacy of past climate fluctuations. Our current and most recent geological time period, the Quaternary, has been characterised by cycles of global climatic and environmental change that have shifted sea levels and led to extensive expansion and recession of glacial ice sheets. In mountain systems, but also elsewhere, this has driven species to undergo alternating bouts of expansion and contraction, as species tracked their increasing or shrinking habitats, respectively. While there is numerous evidence that species both migrated and adapted in response to these climate fluctuations, the majority of studies that have assessed the legacy of past climate evaluated these responses (i.e. range shifts and expansions, or adaptation) in isolation. Hence, it remains unclear how range shift and expansion dynamics interact with adaptive processes in natural populations, especially under heterogenous landscapes. Here, we re-sequence and analyse ca. 1300 individuals of the plant Dianthus sylvestris, sampled across the species’ natural distribution range in the European mountain ranges, to evaluate this. By identifying the species’ glacial refugias and reconstructing post-glacial expansion dynamics based on distribution modelling, past climate models and the species’ patterns of neutral and environment-associated genetic variation, we highlight a tightly-linked co-response of migration and adaptation under climate-induced range expansions; and demonstrate that adaptive processes naturally emerge from climate-induced range expansions across heterogenous landscapes such as the Alps. We show that this is due to shifts in the spatial sorting of adaptive alleles through time, as the species expanded out of geographically restricted glacial refugia and into the broader range of habitats available in the present-day interglacial. These legacies of past climate fluctuations on genetic variation highlight the importance of past evolutionary and phylogeographic reconstructions in understanding and evaluating the patterns of adaptive variation we see in species today.
Reconstructions of past patterns of adaptive variation together with their sequence of recruitment through time provide valuable insights into the environmental and evolutionary processes that shape adaptive variation, and further, provide the evolutionary and phylogeographic contexts necessary to probe the origins and genetic basis of adaptation. In Chapter III, we leverage off our phylogeographic reconstructions in Chapter II and the methodological framework developed in Chapter I to elucidate the genetic basis of elevational adaptation in Dianthus sylvestris and a closely related species, Dianthus carthusianorum, in the historical context of the clade’s rapid radiation ca. 1-2 million years ago (Mya). We show a strong genetic basis underlying observed phenotypic differences between populations of different elevations, characterised by large-effect haplotypes underlying flowering time and potentially frost tolerance. Between species, we find instances of gene-level adaptive convergence between the two species - alluding to introgression and porous genomes across lineages of the radiation, or a rich substrate of ancient genetic variation - but also distinct architectures elsewhere e.g. underlying flowering time. Notably, we infer key adaptive variants to have originated through the recombination of ancestral, divergent haplotypes pre-dating the formation of the species; before being recruited and maintained across lineages of the radiation. Our results reveal that the genomic potential generated through the recombination of adaptive variation across the radiation’s lineages facilitated expansion of species ranges during past climate warming, and may foster evolutionary rescue of contemporary high-elevation populations under future climate change.
The elucidation of adaptive and evolutionary processes in this thesis emphasise the key roles past climatic processes had on species, both in dictating their current distributions and in shaping neutral and adaptive genetic variation. Given that the potential of species to adapt to different environmental conditions is conferred by their extant pool of genetic variation, this highlights species’ reliance on the genetic legacies of the past to respond to future environmental changes. Show more
Permanent link
https://doi.org/10.3929/ethz-b-000541913Publication status
publishedExternal links
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Contributors
Examiner: Widmer, Alexander
Examiner: Wegmann, Daniel
Examiner: Fior, Simone
Examiner: Koch, Marcus
Publisher
ETH ZurichSubject
Population genetics; Ecological genetics; Evolutionary biologyOrganisational unit
03706 - Widmer, Alexander / Widmer, Alexander
Funding
182675 - Ecological Genomics of Plant Adaptation (SNF)
160123 - Genomics of adaptation in the context of a rapid plant radiation (SNF)
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