Genetic legacies of past climate change on Arctic species: how past responses shape future impacts

Major ecosystem changes are under way in the rapidly warming Arctic region. Sea ice loss and tundra shrub expansion are leading to ecological impacts across multiple biological, spatial, and temporal scales. The distribution and population dynamics of reindeer/caribou (Rangifer tarandus L.) — the most numerous and widespread large herbivore in the Arctic — and the dwarf birches (Betula nana L. and Betula glandulosa Michx.) — dominant tundra shrubs — will be affected. Understanding how these species responded to rapid and large-scale climate and sea ice changes in the past will increase our understanding of the long-term ecological and evolutionary implications of anthropogenic climate change. The impacts of past climate change on species leave genetic imprints in their living descendants, which, in turn, influence their genetic variation and capacity to adapt to future changes.
In this thesis, I aim to uncover how climate fluctuations in the Quaternary period (2.6 million years ago - present) shaped the population history of reindeer and the dwarf birches, to improve our understanding of ecological and evolutionary responses to past climate change. I analyse the contemporary genetic variation of these panarctic species in a phylogeographic approach. I model their population history and compare timings of inferred population events with those of climate and environmental changes using paleoenvironmental data. I then explore how the genetic legacies of past climate change impact responses to ongoing climate change in the dwarf birches, in the form of vegetation greening trends associated with the expansion of tundra shrubs. The thesis addresses this aim in three studies presented as research papers.
The first paper, ‘Retracing the response of reindeer to postglacial climate change in Arctic islands’, compares reindeer population history and role of sea ice and ice sheet dynamics in postglacial island colonisation across two regions in the Arctic: the North American islands, and the Barents Sea islands. Using extant reindeer genetic variation, I modelled past population dynamics and tested hypotheses of glacial locations and postglacial dispersal. From the best supported models, I compared the timings of population isolation (genetic divergence) and connectivity (genetic admixture) with reconstructed and modelled changes in sea ice cover, glacial ice sheet dynamics, and other records of past environmental change. I found that the best supported model suggested postglacial dispersal onto deglaciated Arctic islands from continental glacial locations, with modelled divergence times broadly in agreement with fossil data. Sea ice changes often coincided with population events, with differing impacts in the two geographically different systems. The compiled evidence suggests that ice sheet retreat, sea ice concentration, and ocean currents appear to be important influences on postglacial reindeer history and genetic structure in Arctic islands.
The second paper, ‘Molecular footprints of Quaternary climate fluctuations in the circumpolar tundra shrub dwarf birch’, uses similar phylogeographical methods to the first paper, but with a novel genome-wide genetic dataset compiled across the geographical range of the dwarf birches. I compared the timing of population divergence and admixture with the ice sheet configuration obtained from published reconstructions, and used published pollen, macrofossil, and sedimentary DNA (sedaDNA) records to externally evaluate the demographic events inferred from the dwarf birches’ present genetic configuration. The best supported model suggested a Mid-Quaternary origin of the dwarf birch species complex, likely in response to the global cooling and associated large climatic changes of the Mid-Pleistocene Transition. The results identified two distinct genetic groups in Betula glandulosa for the first time, which likely reflect glacial isolation north and south of the North American ice sheets. Population events were coeval with major climatic transitions, with interactions between ice sheet changes, climatic and environmental conditions in ice-free areas, and geographical constraints likely resulting in a complex population history. The results suggest that tundra shrubs such as the dwarf birches may have had more nuanced responses to past climatic changes than previously suggested, with implications for future eco-evolutionary responses to anthropogenic climate change.
The third paper, ‘Arctic greening patterns reflect genetic legacies of glacial refugia and past climate change’ used the ongoing tundra shrub expansion trends, as measured by remotely sensed vegetation greening, as an opportunity to test whether the impacts of past climate change on the genetic structure of the dwarf birches may be influencing their response to contemporary climate change. I tested the association between population-level dwarf birch genetic diversity and genetic admixture, time since glacial ice sheet retreat, contemporary climate, and regional greening trends of the Arctic tundra and high latitude treeless areas. By modelling the relative importance of these factors, I was able to determine that landscape history and genetic diversity in the form of historical genetic admixture are important but previously neglected components of high latitude vegetation greening trends. The relationship between greening trends and genetic diversity suggests that Arctic shrub expansion may be an adaptive response to climate change, and that future evolutionary potential may therefore be modulated by responses to past climate change.
Overall, this thesis demonstrates that postglacial climate change and glacial cycles influenced the evolution and population history of reindeer and the dwarf birches. Climatic fluctuations variously drove population isolation and connectivity. The impacts of these processes included driving allopatric speciation, generating diverse genetic lineages in different regions, enabling dispersal into deglaciated areas, and restoring connectivity between divergent lineages. Species responses were complex, with similar climatic processes resulting in different effects depending on geographical and temporal context. Finally, Arctic species responses to past climate change may impact their future population dynamics and evolution by influencing their contemporary genetic structure and adaptive potential, as illustrated by the link between the population history, genetic structure of the dwarf birches, and their response to ongoing climate change in the form of tundra vegetation greening. Reconstructing past species dynamics in relation to paleoclimatic changes is a useful aid for helping us understand the long-term ecological and evolutionary impacts of environmental change.

Keywords: Arctic
Betula glandulosa
Betula
climate change
Betula nana
dwarf birch
glaciation
Approximate Bayesian computation
demographic history
postglacial dispersal
RADSeq
reindeer
tundra greening
phylogeography
Pleistocene
shrub expansion
sea ice
glacial refugia
refugia
dwarf shrub
Quaternary
ice sheets
demographic modelling
Rangifer tarandus
EVI
caribou
tundra shrub
intraspecific genetic diversity
Advisor: Macias Fauria, M
Saupe, E