To the Caribbean and Beyond: Complete Mitogenomes of Ancient Guinea Pigs (Cavia porcellus) as a proxy for Interaction in the Late Ceramic Age.

The late ceramic age in the Caribbean occurred from AD500 and was associated with increased interaction between the islands and mainland South America. The domestic guinea pig (Cavia porcellus) was introduced to the Caribbean post-AD500 through human transportation, along with the peccary, agouti, armadillo and opossum. The main goal of this thesis was to use guinea pigs as a commensal model to identify likely human migration routes and interaction spheres within the wider Caribbean region, using complete mitogenomes of ancient guinea pigs. Furthermore, the thesis aimed to identify the number of guinea pig introductions to the Caribbean and locate the origins of early historic European and North American guinea pigs. A total of 23 ancient and two modern complete mitogenomes were obtained. The identified haplogroups indicate that two introductions of guinea pigs to the Caribbean occurred, and that ancient Caribbean guinea pigs were most closely related to those from Peru. The first introduction occurred through previously established trade networks from coastal Colombia to Puerto Rico. A second introduction occurred post-AD1000 to the southern Lesser Antilles, likely as a result of coastal migrations through Peru and the northern coasts of Colombia and Venezuela into the Caribbean. In addition, a potential origin for European domestic guinea pigs was found to be in the Andean region encompassing southern Peru and northern Bolivia. A historic period North American guinea pig was found to have come from the Caribbean. Furthermore, it was identified that there may have been two domestication events on the mainland of South America, which contributed to the current population of domestic guinea pigs. This study is the first to use next-generation sequencing to obtain complete mitogenomes of a commensal animal to investigate prehistoric interaction in the pan-Caribbean region, and results are in agreement with current archaeological and genetic evidence for human mobility into the Caribbean

Ancient reindeer mitogenomes reveal island-hopping colonisation of the Arctic archipelagos

Climate warming at the end of the last glacial period had profound effects on the distribution of cold-adapted species. As their range shifted towards northern latitudes, they were able to colonise previously glaciated areas, including remote Arctic islands. However, there is still uncertainty about the routes and timing of colonisation. At the end of the last ice age, reindeer/caribou (Rangifer tarandus) expanded to the Holarctic region and colonised the archipelagos of Svalbard and Franz Josef Land. Earlier studies have proposed two possible colonisation routes, either from the Eurasian mainland or from Canada via Greenland. Here, we used 174 ancient, historical and modern mitogenomes to reconstruct the phylogeny of reindeer across its whole range and to infer the colonisation route of the Arctic islands. Our data shows a close affinity among Svalbard, Franz Josef Land and Novaya Zemlya reindeer. We also found tentative evidence for positive selection in the mitochondrial gene ND4, which is possibly associated with increased heat production. Our results thus support a colonisation of the Eurasian Arctic archipelagos from the Eurasian mainland and provide some insights into the evolutionary history and adaptation of the species to its High Arctic habitat

Ancient Faunal History Revealed by Interdisciplinary Biomolecular Approaches

Starting four decades ago, studies have examined the ecology and evolutionary dynamics of populations and species using short mitochondrial DNA fragments and stable isotopes. Through technological and analytical advances, the methods and biomolecules at our disposal have increased significantly to now include lipids, whole genomes, proteomes, and even epigenomes. At an unprecedented resolution, the study of ancient biomolecules has made it possible for us to disentangle the complex processes that shaped the ancient faunal diversity across millennia, with the potential to aid in implicating probable causes of species extinction and how humans impacted the genetics and ecology of wild and domestic species. However, even now, few studies explore interdisciplinary biomolecular approaches to reveal ancient faunal diversity dynamics in relation to environmental and anthropogenic impact. This review will approach how biomolecules have been implemented in a broad variety of topics and species, from the extinct Pleistocene megafauna to ancient wild and domestic stocks, as well as how their future use has the potential to offer an enhanced understanding of drivers of past faunal diversity on Earth

Integrating multi-taxon palaeogenomes and sedimentary ancient DNA to study past ecosystem dynamics

Ancient DNA (aDNA) has played a major role in our understanding of the past. Important advances in the sequencing and analysis of aDNA from a range of organisms have enabled a detailed understanding of processes such as past demography, introgression, domestication, adaptation and speciation. However, to date and with the notable exception of microbiomes and sediments, most aDNA studies have focused on single taxa or taxonomic groups, making the study of changes at the community level challenging. This is rather surprising because current sequencing and analytical approaches allow us to obtain and analyse aDNA from multiple source materials. When combined, these data can enable the simultaneous study of multiple taxa through space and time, and could thus provide a more comprehensive understanding of ecosystem-wide changes. It is therefore timely to develop an integrative approach to aDNA studies by combining data from multiple taxa and substrates. In this review, we discuss the various applications, associated challenges and future prospects of such an approach

Population dynamics and demographic history of Eurasian collared lemmings.

BACKGROUND: Ancient DNA studies suggest that Late Pleistocene climatic changes had a significant effect on population dynamics in Arctic species. The Eurasian collared lemming (Dicrostonyx torquatus) is a keystone species in the Arctic ecosystem. Earlier studies have indicated that past climatic fluctuations were important drivers of past population dynamics in this species. RESULTS: Here, we analysed 59 ancient and 54 modern mitogenomes from across Eurasia, along with one modern nuclear genome. Our results suggest population growth and genetic diversification during the early Late Pleistocene, implying that collared lemmings may have experienced a genetic bottleneck during the warm Eemian interglacial. Furthermore, we find multiple temporally structured mitogenome clades during the Late Pleistocene, consistent with earlier results suggesting a dynamic late glacial population history. Finally, we identify a population in northeastern Siberia that maintained genetic diversity and a constant population size at the end of the Pleistocene, suggesting suitable conditions for collared lemmings in this region during the increasing temperatures associated with the onset of the Holocene. CONCLUSIONS: This study highlights an influence of past warming, in particular the Eemian interglacial, on the evolutionary history of the collared lemming, along with spatiotemporal population structuring throughout the Late Pleistocene

Investigating the impacts of Late Pleistocene climate change on Arctic mammals using palaeogenomics

The climatic fluctuations of the Late Pleistocene likely had a large impact on the evolutionary history of Arctic species. Palaeogenomics is a useful tool to shed light on how past populations responded to these climatic shifts and the associated ice sheet dynamics and sea level change. Here, I have used modern and ancient DNA data from four Arctic mammals in order to investigate the impacts of Late Pleistocene climate on their evolutionary histories, from population dynamics and demography, to speciation and gene flow, adaptation, and genome erosion. In Paper I, using ancient mitogenomes from across their Late Pleistocene range, I showed that the Eurasian collared lemming (Dicrostonyx torquatus) had a dynamic Late Pleistocene population structure in Europe. Furthermore, the Eemian interglacial likely led to a bottleneck in collared lemmings, after which the species diversified during the Last Glacial period. Nuclear genome data from a modern individual in northeastern Siberia suggests population stability in northeastern Siberia during the Holocene. In Paper II, I sequenced the nuclear genome of a ~18,500 year old woolly rhinoceros (Coelodonta antiquitatis) and used this in combination with mitochondrial data to explore the demographic history of the species. There was little geographic structuring in the northeast Siberian population, and stability in their effective population size just prior to extinction, which may indicate a subsequent rapid decline towards extinction, likely associated with the Bølling-Allerød interstadial. Additionally, I found that this species had mutations in TRPA1, a gene involved in temperature sensitivity. In a third study (Paper III), I used whole genome data from modern and ancient true lemmings (Lemmus sp.) to determine that the Norwegian lemming (L. lemmus) has one of the youngest speciation times (~37-34 ka BP) of mammals. Norwegian lemmings have mutations in genes involved in coat colour, colour perception, fat transport and reproduction, and likely evolved their unique colouration as a result of isolation after the recolonisation of Fennoscandia. Finally, we examined the consequences of long-term small effective population size in muskox (Ovibos moschatus) using 107 modern nuclear genomes and one 21,000 year old Siberian genome (Paper IV). While muskox survived the warming at the end of the Late Pleistocene, the successive founder events experienced during its colonisation of the Canadian Arctic and Greenland reduced the genetic diversity to some of the lowest values observed in mammals. However, the results suggest that the long-term small population size likely led to purging of strongly deleterious alleles in the muskox, allowing them to persist to today with limited evidence of inbreeding depression. From a technical point, this thesis presents four de-novo genome assemblies, and the first whole nuclear genomes for these Arctic species. Taken together, the results in this thesis show that the climatic fluctuations, in particular the Eemian interglacial and Bølling-Allerød interstadial, along with sea level change and the formation and retreat of ice sheets during the Last Glacial Maximum have influenced the evolutionary histories of these four Arctic mammals

Investigating the impacts of Late Pleistocene climate change on Arctic mammals using palaeogenomics

The climatic fluctuations of the Late Pleistocene likely had a large impact on the evolutionary history of Arctic species. Palaeogenomics is a useful tool to shed light on how past populations responded to these climatic shifts and the associated ice sheet dynamics and sea level change. Here, I have used modern and ancient DNA data from four Arctic mammals in order to investigate the impacts of Late Pleistocene climate on their evolutionary histories, from population dynamics and demography, to speciation and gene flow, adaptation, and genome erosion. In Paper I, using ancient mitogenomes from across their Late Pleistocene range, I showed that the Eurasian collared lemming (Dicrostonyx torquatus) had a dynamic Late Pleistocene population structure in Europe. Furthermore, the Eemian interglacial likely led to a bottleneck in collared lemmings, after which the species diversified during the Last Glacial period. Nuclear genome data from a modern individual in northeastern Siberia suggests population stability in northeastern Siberia during the Holocene. In Paper II, I sequenced the nuclear genome of a ~18,500 year old woolly rhinoceros (Coelodonta antiquitatis) and used this in combination with mitochondrial data to explore the demographic history of the species. There was little geographic structuring in the northeast Siberian population, and stability in their effective population size just prior to extinction, which may indicate a subsequent rapid decline towards extinction, likely associated with the Bølling-Allerød interstadial. Additionally, I found that this species had mutations in TRPA1, a gene involved in temperature sensitivity. In a third study (Paper III), I used whole genome data from modern and ancient true lemmings (Lemmus sp.) to determine that the Norwegian lemming (L. lemmus) has one of the youngest speciation times (~37-34 ka BP) of mammals. Norwegian lemmings have mutations in genes involved in coat colour, colour perception, fat transport and reproduction, and likely evolved their unique colouration as a result of isolation after the recolonisation of Fennoscandia. Finally, we examined the consequences of long-term small effective population size in muskox (Ovibos moschatus) using 107 modern nuclear genomes and one 21,000 year old Siberian genome (Paper IV). While muskox survived the warming at the end of the Late Pleistocene, the successive founder events experienced during its colonisation of the Canadian Arctic and Greenland reduced the genetic diversity to some of the lowest values observed in mammals. However, the results suggest that the long-term small population size likely led to purging of strongly deleterious alleles in the muskox, allowing them to persist to today with limited evidence of inbreeding depression. From a technical point, this thesis presents four de-novo genome assemblies, and the first whole nuclear genomes for these Arctic species. Taken together, the results in this thesis show that the climatic fluctuations, in particular the Eemian interglacial and Bølling-Allerød interstadial, along with sea level change and the formation and retreat of ice sheets during the Last Glacial Maximum have influenced the evolutionary histories of these four Arctic mammals

To the Caribbean and Beyond: Complete Mitogenomes of Ancient Guinea Pigs (Cavia porcellus) as a proxy for Interaction in the Late Ceramic Age.

The late ceramic age in the Caribbean occurred from AD500 and was associated with increased interaction between the islands and mainland South America. The domestic guinea pig (Cavia porcellus) was introduced to the Caribbean post-AD500 through human transportation, along with the peccary, agouti, armadillo and opossum. The main goal of this thesis was to use guinea pigs as a commensal model to identify likely human migration routes and interaction spheres within the wider Caribbean region, using complete mitogenomes of ancient guinea pigs. Furthermore, the thesis aimed to identify the number of guinea pig introductions to the Caribbean and locate the origins of early historic European and North American guinea pigs. A total of 23 ancient and two modern complete mitogenomes were obtained. The identified haplogroups indicate that two introductions of guinea pigs to the Caribbean occurred, and that ancient Caribbean guinea pigs were most closely related to those from Peru. The first introduction occurred through previously established trade networks from coastal Colombia to Puerto Rico. A second introduction occurred post-AD1000 to the southern Lesser Antilles, likely as a result of coastal migrations through Peru and the northern coasts of Colombia and Venezuela into the Caribbean. In addition, a potential origin for European domestic guinea pigs was found to be in the Andean region encompassing southern Peru and northern Bolivia. A historic period North American guinea pig was found to have come from the Caribbean. Furthermore, it was identified that there may have been two domestication events on the mainland of South America, which contributed to the current population of domestic guinea pigs. This study is the first to use next-generation sequencing to obtain complete mitogenomes of a commensal animal to investigate prehistoric interaction in the pan-Caribbean region, and results are in agreement with current archaeological and genetic evidence for human mobility into the Caribbean