Investigating evolutionary processes using ancient and historical DNA of rodent species

The Late Quaternary has been a period of significant change for terrestrial mammals, including episodes of extinction, population sub-division and colonisation. Studying this period provides a means to improve understanding of evolutionary mechanisms, and to determine processes that have led to current distributions. For large mammals, recent work has demonstrated the utility of ancient DNA in understanding demographic change and phylogenetic relationships, largely through well-preserved specimens from permafrost and deep cave deposits. In contrast, much less ancient DNA work has been conducted on small mammals. This project focuses on the development of ancient mitochondrial DNA datasets to explore the utility of rodent ancient DNA analysis. Two studies in Europe investigate population change over millennial timescales. Arctic collared lemming (Dicrostonyx torquatus) specimens are chronologically sampled from a single cave locality, Trou Al’Wesse (Belgian Ardennes). Two end Pleistocene population extinction-recolonisation events are identified and correspond temporally with - localised disappearance of the woolly mammoth (Mammuthus primigenius). A second study examines postglacial histories of European water voles (Arvicola), revealing two temporally distinct colonisation events in the UK. Two further studies of Caribbean rodent species assess DNA recovery from more recent, yet highly degraded, material. The Hispaniolan hutia (Plagiodontia aedium), one of the few remaining endemic Caribbean land mammals, is found to represent three distinct lineages, biogeographically consistent with the island’s Cenozoic origins and geographic heterogeneity. The extinct Antillean rice rats (Oryzomyini) were once endemic throughout the Lesser Antilles. Phylogenetic analysis of zooarchaeological rice rat material recovered from across the Lesser Antillean reveals a new genus of rice rat and at least two separate colonisation events, via over water dispersal, from South America. These overall findings demonstrate the utility of ancient rodent DNA in eliciting individual response patterns across rodent species and exploring topics of wider evolutionary interest

The Small and the Dead: A Review of Ancient DNA Studies Analysing Micromammal Species

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Divergent evolutionary processes associated with colonization of offshore islands

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Avelines's Hole: An Unexpected Twist in the Tale

Aveline’s Hole is the largest known Early Mesolithic cemetery in Britain, previously thought to have no evidence for subsequent burial activity. Thus, it came as some surprise when the results of a recent ancient human DNA study found that, of four individuals from the site yielding genomic data, two showed high levels of ancestry from Early Neolithic Aegean farmers. Radiocarbon dating confirmed that these two individuals were indeed British Early Neolithic in date, while the other two had the expected ‘Western Hunter-Gatherer’ ancestry genomic signatures, with the two groups separated in time by nearly five millennia. Moreover, the two Neolithic samples were both crania, while the two Mesolithic samples were long bones. Given the absence of Neolithic dates in the previous sizeable dating programme combined with the difficult history of the collection, i.e., the WWII bombing of its Bristol repository, this raised the question of whether the crania might in fact be from another site. As we show in this paper, a very strong case can be made that the crania do in fact originate from Aveline’s Hole. Additional radiocarbon dating (14 in total, including the above mentioned four) suggests that about half the cranial elements from the site fall within the Early Neolithic, though there is still no evidence for the deposition of post-cranial remains at this time, nor is there any burial evidence in the long intervening period between the Early Mesolithic and the Early Neolithic. Intriguingly, craniometric analyses of legacy data including three crania lost in the bombing suggest that one, Aveline’s Hole ‘A’, may be Upper Palaeolithicin date. As part of this re-investigation of the human remains from the site, we present new stable carbon and nitrogen isotope analyses that differ significantly from those originally reported for the Early Mesolithic, with the new results more in keeping with other isotopic data for this period. We also present new stable carbon and nitrogen isotope results on human remains from the nearby Early Mesolithic sites of Badger Hole and Greylake, and report new Early Mesolithic radiocarbon dates and isotopic data from Cannington Park Quarry. Clear isotopic differences between the Early Mesolithic and the Neolithic remains can be seen, but these are argued to relate primarily to shifts in the underlying ecological baselines, rather than to differences in types of foods consumed (with the caveat that terrestrial wild and domesticated foods will be isotopically similar). The genetic data are summarised, giving evidence not only of the ancestry of Mesolithic and Neolithic individuals from Aveline’s Hole, but also suggesting something of their physical appearance. The degree of population replacement now indicated by ancient DNA suggests that there was a substantial migration of farmers into Britain at the start of the Neolithic. This new information demonstrates the archaeological importance of Aveline's Hole for both the Mesolithic and Neolithic periods."Funding for nine of the new radiocarbon dates from Aveline’s Hole reported here was provided by NERC’s NRCF programme (NF/2016/2/16). The ancient DNA study was funded by the Wellcome Trust (100713/Z/12/Z), as were three new radiocarbon dates from Aveline’s Hole. The isotopic analysis of the Badger Hole human remains was funded as part of a NERC studentship (NE/K500987/1)."https://www.ubss.org.uk/resources/proceedings/vol28/UBSS_Proc_28_1_9-63.pd

Genomic insights into the conservation status of the world’s last remaining Sumatran rhinoceros populations

Highly endangered species like the Sumatran rhinoceros are at risk from inbreeding. Five historical and 16 modern genomes from across the species range show mutational load, but little evidence for local adaptation, suggesting that future inbreeding depression could be mitigated by assisted gene flow among populations. Small populations are often exposed to high inbreeding and mutational load that can increase the risk of extinction. The Sumatran rhinoceros was widespread in Southeast Asia, but is now restricted to small and isolated populations on Sumatra and Borneo, and most likely extinct on the Malay Peninsula. Here, we analyse 5 historical and 16 modern genomes from these populations to investigate the genomic consequences of the recent decline, such as increased inbreeding and mutational load. We find that the Malay Peninsula population experienced increased inbreeding shortly before extirpation, which possibly was accompanied by purging. The populations on Sumatra and Borneo instead show low inbreeding, but high mutational load. The currently small population sizes may thus in the near future lead to inbreeding depression. Moreover, we find little evidence for differences in local adaptation among populations, suggesting that future inbreeding depression could potentially be mitigated by assisted gene flow among populations

Sex-biased parental care and sexual size dimorphism in a provisioning arthropod

The diverse selection pressures driving the evolution of sexual size dimorphism (SSD) have long been debated. While the balance between fecundity selection and sexual selection has received much attention, explanations based on sex-specific ecology have proven harder to test. In ectotherms, females are typically larger than males, and this is frequently thought to be because size constrains female fecundity more than it constrains male mating success. However, SSD could additionally reflect maternal care strategies. Under this hypothesis, females are relatively larger where reproduction requires greater maximum maternal effort – for example where mothers transport heavy provisions to nests. To test this hypothesis we focussed on digger wasps (Hymenoptera: Ammophilini), a relatively homogeneous group in which only females provision offspring. In some species, a single large prey item, up to 10 times the mother’s weight, must be carried to each burrow on foot; other species provide many small prey, each flown individually to the nest. We found more pronounced female-biased SSD in species where females carry single, heavy prey. More generally, SSD was negatively correlated with numbers of prey provided per offspring. Females provisioning multiple small items had longer wings and thoraxes, probably because smaller prey are carried in flight. Despite much theorising, few empirical studies have tested how sex-biased parental care can affect SSD. Our study reveals that such costs can be associated with the evolution of dimorphism, and this should be investigated in other clades where parental care costs differ between sexes and species

First large-scale quantification study of DNA preservation in insects from natural history collections using genome-wide sequencing

Insect declines are a global issue with significant ecological and economic ramifications. Yet, we have a poor understanding of the genomic impact these losses can have. Genome-wide data from historical specimens have the potential to provide baselines of population genetic measures to study population change, with natural history collections representing large repositories of such specimens. However, an initial challenge in conducting historical DNA data analyses is to understand how molecular preservation varies between specimens. Here, we highlight how Next-Generation Sequencing methods developed for studying archaeological samples can be applied to determine DNA preservation from only a single leg taken from entomological museum specimens, some of which are more than a century old. An analysis of genome-wide data from a set of 113 red-tailed bumblebee Bombus lapidarius specimens, from five British museum collections, was used to quantify DNA preservation over time. Additionally, to improve our analysis and further enable future research, we generated a novel assembly of the red-tailed bumblebee genome. Our approach shows that museum entomological specimens are comprised of short DNA fragments with mean lengths below 100 base pairs (BP), suggesting a rapid and large-scale post-mortem reduction in DNA fragment size. After this initial decline, however, we find a relatively consistent rate of DNA decay in our dataset, and estimate a mean reduction in fragment length of 1.9 bp per decade. The proportion of quality filtered reads mapping to our assembled reference genome was around 50%, and decreased by 1.1% per decade. We demonstrate that historical insects have significant potential to act as sources of DNA to create valuable genetic baselines. The relatively consistent rate of DNA degradation, both across collections and through time, mean that population-level analyses—for example for conservation or evolutionary studies—are entirely feasible, as long as the degraded nature of DNA is accounted for

Dual ancestries and ecologies of the Late Glacial Palaeolithic in Britain

Genetic investigations of Upper Palaeolithic Europe have revealed a complex and transformative history of human population movements and ancestries, with evidence of several instances of genetic change across the European continent in the period following the Last Glacial Maximum (LGM). Concurrent with these genetic shifts, the post-LGM period is characterized by a series of significant climatic changes, population expansions and cultural diversification. Britain lies at the extreme northwest corner of post-LGM expansion and its earliest Late Glacial human occupation remains unclear. Here we present genetic data from Palaeolithic human individuals in the United Kingdom and the oldest human DNA thus far obtained from Britain or Ireland. We determine that a Late Upper Palaeolithic individual from Gough's Cave probably traced all its ancestry to Magdalenian-associated individuals closely related to those from sites such as El Mirón Cave, Spain, and Troisième Caverne in Goyet, Belgium. However, an individual from Kendrick's Cave shows no evidence of having ancestry related to the Gough’s Cave individual. Instead, the Kendrick’s Cave individual traces its ancestry to groups who expanded across Europe during the Late Glacial and are represented at sites such as Villabruna, Italy. Furthermore, the individuals differ not only in their genetic ancestry profiles but also in their mortuary practices and their diets and ecologies, as evidenced through stable isotope analyses. This finding mirrors patterns of dual genetic ancestry and admixture previously detected in Iberia but may suggest a more drastic genetic turnover in northwestern Europe than in the southwest

Ancient genomes indicate population replacement in Early Neolithic Britain

The roles of migration, admixture and acculturation in the European transition to farming have been debated for over 100 years. Genome-wide ancient DNA studies indicate predominantly Aegean ancestry for continental Neolithic farmers, but also variable admixture with local Mesolithic hunter-gatherers. Neolithic cultures first appear in Britain circa 4000 bc, a millennium after they appeared in adjacent areas of continental Europe. The pattern and process of this delayed British Neolithic transition remain unclear. We assembled genome-wide data from 6 Mesolithic and 67 Neolithic individuals found in Britain, dating 8500–2500 bc. Our analyses reveal persistent genetic affinities between Mesolithic British and Western European hunter-gatherers. We find overwhelming support for agriculture being introduced to Britain by incoming continental farmers, with small, geographically structured levels of hunter-gatherer ancestry. Unlike other European Neolithic populations, we detect no resurgence of hunter-gatherer ancestry at any time during the Neolithic in Britain. Genetic affinities with Iberian Neolithic individuals indicate that British Neolithic people were mostly descended from Aegean farmers who followed the Mediterranean route of dispersal. We also infer considerable variation in pigmentation levels in Europe by circa 6000 bc