The spatial genetic structure of Martino's vole, a rare palaeoendemic species of the western Balkans, was investigated using DNA isolated from archived museum samples. The study was based on partial sequencing (555 bp) of the mitochondrial cytochrome b gene for 63 specimens from 20 different localities throughout the species' range. Three highly divergent allopatric phylogenetic lineages (Northwestern, Central and Southeastern) were recognized among 47 haplotypes, suggesting three independent glacial differentiation centres within the western Balkans. The Northwestern lineage, which showed the highest divergence from all other samples (mean sequence divergence of 6.64% +/- 1.10), comprised samples collected from northwest of the Neretva River in Croatia, western Bosnia and Herzegovina. The Central and Southeastern lineages were separated by an average sequence divergence of 2.95% +/- 0.66 and were geographically divided by the Drim River (the Kosovo Basin in Serbia). Overall, haplotype diversity decreased from the Northwestern lineage to the Central and subsequently the Southeastern lineage, in a geographical pattern consistent with a stepping stone colonization. The observed distribution indicates a gradual southerly expansion with subsequent allopatry across the Neretva River and Drim River approximately 1 and 0.3 million years ago, respectively. Such a scenario is concordant with palaeontological evidence. Several highly divergent sublineages within the Northwestern and Central lineages showed no significant geographical structuring, suggesting secondary contact of allopatrically evolved lineages. We hypothesize that the topographical complexity of the Balkans promoted allopatry and isolation on a small geographical scale during interglacial periods, with secondary contact during glacial maxima. Furthermore, the three main lineages should be regarded as evolutionary significant units with important implications for conservation. Ecological data show that the Northwestern lineage in particular fulfils all criteria for a highly endangered, evolutionarily significant unit.
Traditionally, taxonomic identification has relied upon morphological characters. In the last two decades, molecular tools based on DNA sequences of short standardised gene fragments, termed DNA barcodes, have been developed for species discrimination. The most common DNA barcode used in animals is a fragment of the cytochrome c oxidase (COI) mitochondrial gene, while for plants, two chloroplast gene fragments from the RuBisCo large subunit (rbcL) and maturase K (matK) genes are widely used. Information gathered from DNA barcodes can be used beyond taxonomic studies and will have far-reaching implications across many fields of biology, including ecology (rapid biodiversity assessment and food chain analysis), conservation biology (monitoring of protected species), biosecurity (early identification of invasive pest species), medicine (identification of medically important pathogens and their vectors) and pharmacology (identification of active compounds). However, it is important that the limitations of DNA barcoding are understood and techniques continually adapted and improved as this young science matures.
International initiatives aimed at generating genomic resources, and particularly reference genomes, have flourished in recent years. Some focus on specific taxa, such as the Vertebrate Genomes Project, Bird Genome 10K Project, Bat1K Project, Global Invertebrate Genomics Alliance, 10 000 Plant Genomes Project, and 1000 Fungal Genomes project. Others focus on geographic regions, such as the California Conservation Genomics Project, Darwin Tree of Life for Britain and Ireland, Catalan Initiative for the Earth BioGenome Project in the Catalan territories, Endemixit in Italy, Norwegian Earth Biogenome Project, and SciLifeLab in Sweden, on applications such as the LOEWE Translational Biodiversity Genomics in Germany, or on ecological systems such as the Aquatic Symbiosis Genomics project. Collectively part of the Earth BioGenome Project (EBP), in Europe these initiatives are organized under the umbrella of the European Reference Genome Atlas (ERGA). A genome atlas of European biodiversityERGA is a pan-European scientific response to the current threats to biodiversity. Approximately one fifth of the ~200 000 eukaryotic species present in Europe can be inferred to be at risk of extinction according to the International Union for Conservation of Nature (IUCN) Red List classification (this estimate only considers the assessed species; https://www.iucn.org/regions/europe/our-work/biodiversity-conservation/european-red-list-threatened-species).ERGA aims to generate reference genomes of European eukaryotic species across the tree of life, including threatened, endemic, and keystone species, as well as pests and species important to agriculture, fisheries, and ecosystem function and stability. ERGA builds upon current genomic consortia in EU member states, EU Associated Countries, representatives of other countries within the European bioregion, and international collaborators. These reference genomes will address fundamental and applied questions in conservation, biology, and health. ERGA seeks to alert the EU about the potential of conservation genomics, and particularly the role of reference genomes, in biodiversity assessment, conservation strategies, and restoration efforts.
Comprehensive taxonomic sampling can vastly improve the accuracy of phylogenetic reconstruction. Here, we present the most inclusive phylogenetic analysis of Arvicolinae (Mammalia, Rodentia) to date, combining all published cytochrome b gene sequences of greater than 1097 bp and new sequences from two monotypic genera. Overall, the phylogenetic relationships between 69 species of voles and lemmings, representing 18 genera and 10 tribes, were studied. By applying powerful modern approaches to phylogenetic reconstruction, such as maximum likelihood and Bayesian analysis, we provide new information on the early pulse of evolution within the Arvicolinae. While the position of two highly divergent lineages, Phenacomys and Ondatra, could not be resolved, the tribe Lemmini, appeared as the most basal group of voles. The collared lemmings (Dicrostonychini) grouped together with all of the remaining tribes. The two previously unstudied monotypic genera Dinaromys and Prometheomys form a moderately well-supported monophyletic clade, possibly a sister group to Ellobius (Ellobiusini). Furthermore, with one exception, all tribes (sensu Musser & Carleton, 2005) proved to be monophyletic and can thus be regarded as meaningful evolutionary entities. Only the tribe Arvicolini emerged as paraphyletic in both analyses because of the unresolved phylogenetic position of Arvicola terrestris. Steppe voles of the genus Lagurus were solidly supported as a sister group to the Microtus and allies clade.
The spatial genetic structure of the European ground squirrel, a species characteristic of the short-grass steppe, was investigated on the basis of a 1140-bp cyt b gene sequence. The phylogeographical architecture of this species is expected to shed light on the putative long-term presence of the steppic ecosystem in south-eastern Europe and the evolutionary consequences of glacial cycles as forcing factors in speciation. Among 31 haplotypes, three highly divergent phylogenetic lineages (Southern, Northern and Jakupica) were recognized. This result suggests the past existence of an allopatric fragmentation event caused by effective biogeographical barriers. The Southern lineage consisted of the southernmost populations, those from Greece, Macedonia and European Turkey, and showed the highest divergence from all other samples. Haplotypes of the Northern lineage showed little geographical structure, with dispersal on both sides of the Danube River and in both of the two main geographical fragments of the species. The Jakupica lineage is a geographical isolate on a high plateau in central Macedonia. The estimated time for divergence of the Southern lineage (ca. 0.58 Mya) suggests the long-term persistence of a short-grass steppic refugium in the southern Balkans. Although the divergence between the Northern and Jakupica lineages occurred more recently (ca. 0.3 Mya), it still putatively predates two glacial cycles. The three phylogeographical lineages of the European ground squirrel should be regarded as independent units for conservation management purposes.
The phylogeographic architecture of the common vole, Microtus arvalis, has been well-studied using mitochondrial DNA and used to test hypotheses relating to glacial refugia. The distribution of the five described cytochrome b (cyt b) lineages in Europe west of Russia has been interpreted as a consequence of postglacial expansion from both southern and central European refugia. A recently proposed competing model suggests that the 'cradle' of the M. arvalis lineages is in western central Europe from where they dispersed in different directions after the Last Glacial Maximum. In the present study, we report a new cyt b lineage of the common vole from the Balkans that is not closely related to any other lineage and whose presence might help resolve these issues of glacial refugia. The Balkan phylogroup occurs along the southern distributional border of M. arvalis in central and eastern Bosnia and Herzegovina, Montenegro, and eastern Serbia. Further north and west in Slovenia, Bosnia and Herzegovina, and Serbia, common voles belong to the previously-described Eastern lineage, whereas both lineages are sympatric in one site in Bosnia and Herzegovina. The Balkan phylogroup most reasonably occupied a glacial refugium already known for various Balkan endemic species, in contrast to the recently proposed model. South-east Europe is an absolutely crucial area for understanding the postglacial colonization history of small mammals in Europe and the present study adds to the very few previous detailed phylogeographic studies of this region.
Hybridisation and gene introgression are important sources of diversification, the relevance of which in the evolutionary processes is well recognised. Their fitness consequences in animal populations, however, are not sufficiently well understood, despite hybridisation rates becoming increasingly important worldwide following human‐related activities such as domestication, game management and habitat alteration. In Europe, the density and distribution of native ungulates have largely been influenced by humans since pre‐historic times. This, alongside the introduction of non‐native and domesticated species, may bear major consequences at the genetic and population levels. We provide an updated overview of recent hybridisation events in wild European ungulates; we describe their ecological drivers, extent, current distribution, potential consequences and proposed management strategies. We reviewed the scientific literature published between 2000 and 2018 and found that confirmed hybridisation was described in 75 of the 89 references we included, involving nearly all the species that we investigated. Most researchers relied on genetic information for hybrid identification, which often involved a domestic counterpart. However, introductions and translocations also led to crossbreeding between wild ungulate (sub)species. Only 43 papers provided management recommendations, mostly focused on preventing hybridisation and removing hybrids. Hybridisation proved to be relatively common in several ungulate taxa in Europe. Despite reported changes in phenotype and fitness‐related traits in some species, the consequences of hybridisation for adaptation, life history, and evolutionary potential remain largely unknown. The current conservation paradigm aims to prevent the spread of domestic or non‐native genes in native populations; accordingly, conservation plans should: 1) determine the genetic origin of possible source populations; 2) protect native populations from the risk of crossbreeding with non‐native ones, and 3) establish permanent monitoring.
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