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Inferring demographic history and speciation of grouse using whole genome sequences
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. (Höglund lab)
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

From an ecological perspective, knowledge of demographic history is highly valuable because population size fluctuations can be matched to known climatic events, thereby revealing great insight into a species’ reaction to past climate change. This in turn enables us to predict how they might respond to future climate scenarios. Prominently, with the advent of high-throughput sequencing it is now becoming possible to assemble genomes of non-model organisms thereby providing unprecedented resolution to the study of demographic history and speciation. This thesis utilises four species of grouse (Aves, subfamily Tetraoninae) in order to explore the demographic history and speciation within this lineage; the willow grouse, red grouse, rock ptarmigan and the black grouse. I, and my co-authors, begin by reviewing the plethora of methods used to estimate contemporary effective population size (Ne) and demographic history that are available to animal conservation practitioners. We find that their underlying assumptions and necessary input data can bias in their application, and thus we provide a summary of their applicability.

I then use the whole genomes of the black grouse, willow grouse and rock ptarmigan to infer their population dynamics within the last million years. I find three dominant periods that shape their demographic history: early Pleistocene cooling (3-0.9 Mya), the mid-Brunhes event (430 kya) and the last glacial period (110-10 kya). I also find strong signals of local population history – recolonization and subdivision events – affecting their demography. In the subsequent study, I explore the grouse dynamics within the last glacial period in more detail by including more distant samples and using ecological modelling to track habitat distribution changes. I further uncover strong signals of local population history, with multiple fringe populations undergoing severe bottlenecks. I also determine that future climate change is expected to drastically constrict the distribution of the studied grouse.

Lastly, I use whole genome sequencing to uncover 6 highly differentiated regions, containing 7 genes, hinting at their role in adaptation and speciation in three grouse taxa. I also locate a region of low differentiation, containing the Agouti pigmentation gene, indicating its role in the grouse plumage coloration.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2016. , 49 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1391
Keyword [en]
Demographic history, speciation, effective population size, adaptation, willow grouse, red grouse, black grouse, rock ptarmigan, Tetraoninae, conservation genetics, climate change, PSMC, species distribution modelling, FOXP4, Agouti
National Category
Evolutionary Biology Ecology Genetics
Identifiers
URN: urn:nbn:se:uu:diva-299926ISBN: 978-91-554-9627-2OAI: oai:DiVA.org:uu-299926DiVA: diva2:950335
Public defence
2016-09-16, Lindahlssalen, EBC (Evolutionary Biology Center), Norbyvägen 18B, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2016-08-24 Created: 2016-07-29 Last updated: 2016-08-26
List of papers
1. The utility of effective population size in population management 1:estimating contemporary effective size
Open this publication in new window or tab >>The utility of effective population size in population management 1:estimating contemporary effective size
2016 (English)In: Conservation Genetics, ISSN 1566-0621, E-ISSN 1572-9737Article in journal (Refereed) Submitted
Abstract [en]

Estimates of effective population size (Ne) are highly desirable in managed populations because they are informative of the rate at which genetic variation is being lost through the processes of genetic drift or inbreeding. Due to the notorious difficulty of accurate Ne estimation in natural populations, myriad estimation methods have been developed over the last 50 years. Conservation practitioners and researchers who are unfamiliar with the Ne estimation literature are now faced with an overwhelming amount of choice when selecting an estimation method and, unfortunately, the resources available to help them make this decision rarely consider the practicalities of implementing these methods. This review aims to alleviate this problem by explicitly considering these practicalities while describing and comparing the most popular estimation methods available. We begin by clearly describing how estimates of Ne can be used in population management. We then go on to describe the most popular methods available for Ne estimation, stating the assumptions that are made and the data that are required. The review concludes with recommendations of the most appropriate estimation methods given specific motivations for estimating Ne and the types of data that are practical to collect.

Keyword
Effective population size, genetic drift, genetic variation, population management, conservation genetics
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-295473 (URN)
Available from: 2016-06-07 Created: 2016-06-07 Last updated: 2016-08-26Bibliographically approved
2. The utility of effective population size in population management 2:estimating demographic history
Open this publication in new window or tab >>The utility of effective population size in population management 2:estimating demographic history
2016 (English)In: Conservation Genetics, ISSN 1566-0621, E-ISSN 1572-9737Article in journal (Refereed) Submitted
Abstract [en]

Elucidating demographic history by tracking the fluctuations of effective population size (Ne) through time has helped uncover interesting insight into the ecology and evolutionary history of a wide array of populations and species. This field of research has seen many exciting methods put forth that together can retrieve the demographic history across many time scales and as such, it is becoming a very useful tool available for conservation practitioners. However, due to the inherent difficulties associated with estimating Ne, the literature can be very technical it is often unclear how methods differ in their assumptions and data requirements. Thus, the choice of which method to use for what purpose can be an extremely difficult one. With this review, we aim to first describe the major methods used to estimate demographic history and clarify their underlying requirements and assumptions. We then highlight some of the overarching motives to understand past Ne fluctuations and we conclude with advice about which methods to use to address these specific motives with a particular focus on the temporal resolution required.

Keyword
Effective population size, demographic history, population management, Msvar, PSMC, skyline plot
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-295477 (URN)
Available from: 2016-06-07 Created: 2016-06-07 Last updated: 2016-08-26Bibliographically approved
3. Looking into the past: the reaction of three grouse species to climate change over the last million years using whole genome sequences
Open this publication in new window or tab >>Looking into the past: the reaction of three grouse species to climate change over the last million years using whole genome sequences
2016 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 25, no 2, 570-580 p.Article in journal (Refereed) Published
Abstract [en]

Tracking past population fluctuations can give insight into current levels of genetic variation present within species. Analysing population dynamics over larger timescales can be aligned to known climatic changes to determine the response of species to varying environments. Here, we applied the Pairwise Sequentially Markovian Coalescent (PSMC) model to infer past population dynamics of three widespread grouse species; black grouse, willow grouse and rock ptarmigan. This allowed the tracking of the effective population size (Ne) of all three species beyond 1 Mya, revealing that (i) early Pleistocene cooling (~2.5 Mya) caused an increase in the willow grouse and rock ptarmigan populations, (ii) the mid-Brunhes event (~430 kya) and following climatic oscillations decreased the Ne of willow grouse and rock ptarmigan, but increased the Ne of black grouse and (iii) all three species reacted differently to the last glacial maximum (LGM) – black grouse increased prior to it, rock ptarmigan experienced a severe bottleneck and willow grouse was maintained at large population size. We postulate that the varying PSMC signal throughout the LGM depicts only the local history of the species. Nevertheless, the large population fluctuations in willow grouse and rock ptarmigan indicate that both species are opportunistic breeders while black grouse tracks the climatic changes more slowly and is maintained at lower Ne. Our results highlight the usefulness of the PSMC approach in investigating species’ reaction to climate change in the deep past, but also that caution should be taken in drawing general conclusions about the recent past.

Keyword
climate change, effective population size, pairwise sequentially Markovian coalescent, Pleistocene, Tetraoninae
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-295467 (URN)10.1111/mec.13496 (DOI)000369530000010 ()26607571 (PubMedID)
Available from: 2016-06-07 Created: 2016-06-07 Last updated: 2016-08-26Bibliographically approved
4. Past and potential future dynamics of three grouse species using ecological and whole genome coalescent modelling
Open this publication in new window or tab >>Past and potential future dynamics of three grouse species using ecological and whole genome coalescent modelling
(English)Manuscript (preprint) (Other academic)
Keyword
climate change, demographic history, Pleistocene, PSMC, species distribution modelling, Tetraoninae
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-295480 (URN)
Available from: 2016-06-07 Created: 2016-06-07 Last updated: 2016-08-26
5. Insight into speciation and adaptation in grouse as revealed by whole genome sequencing
Open this publication in new window or tab >>Insight into speciation and adaptation in grouse as revealed by whole genome sequencing
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Understanding the molecular basis of adaption is one of the central goals in evolutionary biology and when investigated across sister species it can provide detailed insight into the mechanisms of speciation. The grouse (subfamily Tetraoninae) constitute an avian lineage whose members inhabit a wide variety of habitats and possess diverse plumage traits and as such offer an interesting case study. Here, we sequence the genomes of 34 individuals comprising three grouse taxa; the willow grouse (Lagopus lagopus lagopus), the red grouse (Lagopus lagopus scoticus) and the rock ptarmigan (Lagopus muta) in order to uncover the genomic architecture of speciation and the genes involved in adaptation. We identify 6 regions, containing 7 genes that show consistent signs of differential selection across the species. These genes are highly involved in a variety of cell processes ranging from stress response to neural, gut, olfactory and limb development. Genome wide neutrality test statistics also reveal a strong signal of population expansion acting across the genomes, which is in line with previous demographic studies in these systems. Additionally, we uncover a 3.5Mb region on chromosome 20 that shows considerably lower levels of differentiation across the three grouse lineages, indicating the action of uniform selection. The Agouti gene, which is integral in the pigmentation pathway, lies at the 5' start of this region hinting at the conserved development of brown plumage across the three taxa. Together, our results provide a key step in the exploration of grouse speciation and adaptation. 

Keyword
Speciation, adaptation, grouse, Tetraoninae, population genomics, FOXP4, Agouti
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-298415 (URN)
Available from: 2016-07-04 Created: 2016-07-04 Last updated: 2016-08-26

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