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Ancient DNA and climatic change: new perspectives from insular environments

Final Report Summary - MEDITADNA (Ancient DNA and climatic change: new perspectives from insular environments)

Ancient DNA (aDNA) studies (i.e. analysis of genetic information from extinct species) have been proven to be an excellent tool to understand several aspects of the biology of animals and plants that became extinct in the near past. In fossil vertebrates, these analyses can provide remarkable information about taxonomy (identify species), phylogenetic relationships (find ancestor-descendant lineage), past population structure, migratory movements, etc.
Another remarkable outcome of reading genetic signatures in aDNA is that they can be a really powerful way to determine the effects of past climate changes on fossil species and to understand and predict the ongoing and future impacts of climate change on biodiversity.
Since the first analysis of genetic data from fossil or sub-fossil remains of vertebrates published in the mid-80’s, aDNA has rapidly developed thanks to the improvements in extraction protocols (obtaining of DNA from bones), and the growing efficiency of the Next Generation Sequencing (NGS) methods now allows the recovery of a vast amount of genetic information that can be analyzed with bioinformatic software. All these advances have allowed the study of sequences obtained from samples with a limited DNA content and found in non-favourable environments for DNA preservation, i.e. areas with relatively humid and warm climates as the Mediterranean islands. The development of new laboratory protocols to increase the yield of DNA from fossil samples, the so-called enrichment techniques, has been a crucial step for the success of this project.
The MEDITADNA project (PIOF-GA-2011-300854, FP7- PEOPLE), has been carried out during the outgoing phase at the Australian Centre for Ancient DNA (ACAD, University of Adelaide, Australia. Supervisor Prof. Alan Cooper) and during the return phase at the Mediterranean Institute for Advanced Studies (IMEDEA, CSIC-UIB, Spain. Supervisor Dr. Joan Pons). This project aimed to study the genetic structure of multiple individuals from the bovid Myotragus balearicus, a fossil dwarf goat-like bovid from the Balearic Islands (Western Mediterranean). This bovid arrived to these islands around 5 My ago, during the so-called Messinian Salinity Crisis (MSC) when the partial desiccation of the Mediterranean basin allowed the migration of several vertebrates from surrounding mainland areas through land bridges. After isolation of these islands, Myotragus survived in this archipelago for more than 5 My, a period of time in which important climate changes occurred. Together with Myotragus, two other genera of mammals survived in the two eastern islands, Mallorca and Menorca: the dormouse Hypnomys (Gliridae; Rodentia) and the shrew Nesiotites (Soricidae; Eulipotyphla). These three lineages survived since its arrival during the MSC until the human arrival to those islands approximately 4,500 years ago (see Figure 1).
Although the objectives of the project were mainly related with the analysis of Myotragus sequences (characterization of populations, understanding the response to climate changes, palaeogenomics, phylogeny, and diet analysis through the fossilized dung or coprolites), the recovery of DNA from the other two extinct mammalian species, Hypnomys and Nesiotites, would provide genetic information for phylogenetic and population analyses.
During the first period at ACAD, the researcher of the project, Pere (Pedro) Bover (perebover@imedea.uib-csic.es) was intensively working in the laboratory facilities. Up to 57 bone samples and 8 coprolites of Myotragus, 3 bones and 2 coprolites of Hypnomys, and 3 bones of Nesiotites from different caves have been extracted. From the Myotragus bone samples 16 yielded endogenous DNA so far, as well as one sample of Hypnomys and one of Nesiotites.
Data coming from the sequencing runs were analysed with updated bioinformatic tools currently available during the second period of the project at IMEDEA.
DNA identified as belonging to Myotragus was obtained from 16 bones of the 57 extracted. All these samples come from caves located at the Northern Mountains (Serra de Tramuntana) of Mallorca. Up to 13 complete or almost complete mitochondrial genomes of M. balearicus were used to carry out phylogenetic analyses, and to evaluate the phylogeographic and population structure of the bovid in this island. The genetic variability observed in these mitochondrial genomes allowed us to investigate the morphological variability displayed by the species, and together with new radiocarbon dates, to suggest some hypotheses about the extinction of the species.
Also informative genetic data (mitochondrial DNA) was used to study the phylogenetic relationships of the fossil shrew (Nesiotites) and dormouse (Hypnomys).
On the other hand, the results of the analysis of DNA content in Myotragus coprolites suggests that the vast majority of the sequences obtained (around 15 millions) were identified as bacterial DNA, including some taxa from gut microbiome. Strikingly, the amount of plant DNA contained in the coprolites was low.
As a big outcome of the project, in addition to the training and skill acquisition by the fellow, we have shown that a remarkable amount of genetic information can be obtained from deposits in areas where climate does not favour the preservation of ancient DNA. In our opinion the project results suppose a huge step towards the understanding of the role of islands as refuge during climate changes, and this kind of “Conservation Paleontology” studies can be used to improve the understanding of current conservation priorities, to improve management and planning. This research ranges from the genetic identification of extinct species and population to guide reintroduction programs, to reconstruct past environments, or to in-depth analyses of the responses of populations to environmental changes (such as climatic or human impacts) over time. In addition these studies have identified a remarkably strong influence of climate change on the biodiversity and distribution of large vertebrates over the past 100,000 years.
The research involved in the proposal will also shed light on the validity of statements that suggest that the reduction of habitat range promotes a loss of genetic diversity.
The methodology and conclusions obtained in this project would be of great applicability to other fossil and extant taxa. This kind of study will provide a framework for understanding potential responses of species to future climate changes, especially in restricted insular species or even in mainland isolated populations due to human-related impacts. This approach has been referred to as “looking backwards to look forwards”.
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