Publications by authors named "Axel Barlow"

32 Publications

Middle Pleistocene genome calibrates a revised evolutionary history of extinct cave bears.

Curr Biol 2021 Feb 9. Epub 2021 Feb 9.

School of Science and Technology, Nottingham Trent University, Clifton Lane, Nottingham NG11 8NS, UK.

Palaeogenomes provide the potential to study evolutionary processes in real time, but this potential is limited by our ability to recover genetic data over extended timescales. As a consequence, most studies so far have focused on samples of Late Pleistocene or Holocene age, which covers only a small part of the history of many clades and species. Here, we report the recovery of a low coverage palaeogenome from the petrous bone of a ∼360,000 year old cave bear from Kudaro 1 cave in the Caucasus Mountains. Analysis of this genome alongside those of several Late Pleistocene cave bears reveals widespread mito-nuclear discordance in this group. Using the time interval between Middle and Late Pleistocene cave bear genomes, we directly estimate ursid nuclear and mitochondrial substitution rates to calibrate their respective phylogenies. This reveals post-divergence mitochondrial transfer as the dominant factor explaining their mito-nuclear discordance. Interestingly, these transfer events were not accompanied by large-scale nuclear introgression. However, we do detect additional instances of nuclear admixture among other cave bear lineages, and between cave bears and brown bears, which are not associated with mitochondrial exchange. Genomic data obtained from the Middle Pleistocene cave bear petrous bone has thus facilitated a revised evolutionary history of this extinct megafaunal group. Moreover, it suggests that petrous bones may provide a means of extending both the magnitude and time depth of palaeogenome retrieval over substantial portions of the evolutionary histories of many mammalian clades.
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http://dx.doi.org/10.1016/j.cub.2021.01.073DOI Listing
February 2021

Ancient DNA from the Asiatic Wild Dog () from Europe.

Genes (Basel) 2021 Jan 22;12(2). Epub 2021 Jan 22.

Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476 Potsdam, Germany.

The Asiatic wild dog (), restricted today largely to South and Southeast Asia, was widespread throughout Eurasia and even reached North America during the Pleistocene. Like many other species, it suffered from a huge range loss towards the end of the Pleistocene and went extinct in most of its former distribution. The fossil record of the dhole is scattered and the identification of fossils can be complicated by an overlap in size and a high morphological similarity between dholes and other canid species. We generated almost complete mitochondrial genomes for six putative dhole fossils from Europe. By using three lines of evidence, i.e., the number of reads mapping to various canid mitochondrial genomes, the evaluation and quantification of the mapping evenness along the reference genomes and phylogenetic analysis, we were able to identify two out of six samples as dhole, whereas four samples represent wolf fossils. This highlights the contribution genetic data can make when trying to identify the species affiliation of fossil specimens. The ancient dhole sequences are highly divergent when compared to modern dhole sequences, but the scarcity of dhole data for comparison impedes a more extensive analysis.
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http://dx.doi.org/10.3390/genes12020144DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7911384PMC
January 2021

Author Correction: Heavy reliance on plants for Romanian cave bears evidenced by amino acid nitrogen isotope analysis.

Sci Rep 2020 Oct 28;10(1):18805. Epub 2020 Oct 28.

Department of Geosciences, Biogeology, University of Tübingen, Hölderlinstraße 12, 72074, Tübingen, Germany.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41598-020-75177-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7591857PMC
October 2020

Ancestral mitogenome capture of the Southeast Asian banded linsang.

PLoS One 2020 30;15(6):e0234385. Epub 2020 Jun 30.

Leibniz Institute for Zoo- and Wildlife Research, Berlin, Germany.

Utilising a reconstructed ancestral mitochondrial genome of a clade to design hybridisation capture baits can provide the opportunity for recovering mitochondrial sequences from all its descendent and even sister lineages. This approach is useful for taxa with no extant close relatives, as is often the case for rare or extinct species, and is a viable approach for the analysis of historical museum specimens. Asiatic linsangs (genus Prionodon) exemplify this situation, being rare Southeast Asian carnivores for which little molecular data is available. Using ancestral capture we recover partial mitochondrial genome sequences for seven banded linsangs (P. linsang) from historical specimens, representing the first intraspecific genetic dataset for this species. We additionally assemble a high quality mitogenome for the banded linsang using shotgun sequencing for time-calibrated phylogenetic analysis. This reveals a deep divergence between the two Asiatic linsang species (P. linsang, P. pardicolor), with an estimated divergence of ~12 million years (Ma). Although our sample size precludes any robust interpretation of the population structure of the banded linsang, we recover two distinct matrilines with an estimated tMRCA of ~1 Ma. Our results can be used as a basis for further investigation of the Asiatic linsangs, and further demonstrate the utility of ancestral capture for studying divergent taxa without close relatives.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0234385PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7326216PMC
August 2020

Heavy reliance on plants for Romanian cave bears evidenced by amino acid nitrogen isotope analysis.

Sci Rep 2020 04 20;10(1):6612. Epub 2020 Apr 20.

Department of Geosciences, Biogeology, University of Tübingen, Hölderlinstraße 12, 72074, Tübingen, Germany.

Heavy reliance on plants is rare in Carnivora and mostly limited to relatively small species in subtropical settings. The feeding behaviors of extinct cave bears living during Pleistocene cold periods at middle latitudes have been intensely studied using various approaches including isotopic analyses of fossil collagen. In contrast to cave bears from all other regions in Europe, some individuals from Romania show exceptionally high δN values that might be indicative of meat consumption. Herbivory on plants with high δN values cannot be ruled out based on this method, however. Here we apply an approach using the δN values of individual amino acids from collagen that offsets the baseline δN variation among environments. The analysis yielded strong signals of reliance on plants for Romanian cave bears based on the δN values of glutamate and phenylalanine. These results could suggest that the high variability in bulk collagen δN values observed among cave bears in Romania reflects niche partitioning but in a general trophic context of herbivory.
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http://dx.doi.org/10.1038/s41598-020-62990-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7170912PMC
April 2020

Hyena paleogenomes reveal a complex evolutionary history of cross-continental gene flow between spotted and cave hyena.

Sci Adv 2020 03 13;6(11):eaay0456. Epub 2020 Mar 13.

Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, 14476 Potsdam, Germany.

The genus (African spotted and Eurasian cave hyenas) includes several closely related extinct and extant lineages. The relationships among these lineages, however, are contentious. Through the generation of population-level paleogenomes from late Pleistocene Eurasian cave hyena and genomes from modern African spotted hyena, we reveal the cross-continental evolutionary relationships between these enigmatic hyena lineages. We find a deep divergence (~2.5 Ma) between African and Eurasian populations, suggesting that ancestral left Africa around the same time as early . Moreover, we find discordance between nuclear and mitochondrial phylogenies and evidence for bidirectional gene flow between African and Eurasian after the lineages split, which may have complicated prior taxonomic classifications. Last, we find a number of introgressed loci that attained high frequencies within the recipient lineage, suggesting some level of adaptive advantage from admixture.
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http://dx.doi.org/10.1126/sciadv.aay0456DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7069707PMC
March 2020

Ancient DNA reveals twenty million years of aquatic life in beavers.

Curr Biol 2020 02;30(3):R110-R111

Institute for Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany.

Xenikoudakis et al. report a partial mitochondrial genome of the extinct giant beaver Castoroides and estimate the origin of aquatic behavior in beavers to approximately 20 million years. This time estimate coincides with the extinction of terrestrial beavers and raises the question whether the two events had a common cause.
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http://dx.doi.org/10.1016/j.cub.2019.12.041DOI Listing
February 2020

Consensify: A Method for Generating Pseudohaploid Genome Sequences from Palaeogenomic Datasets with Reduced Error Rates.

Genes (Basel) 2020 01 2;11(1). Epub 2020 Jan 2.

Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476 Potsdam, Germany.

A standard practise in palaeogenome analysis is the conversion of mapped short read data into pseudohaploid sequences, frequently by selecting a single high-quality nucleotide at random from the stack of mapped reads. This controls for biases due to differential sequencing coverage, but it does not control for differential rates and types of sequencing error, which are frequently large and variable in datasets obtained from ancient samples. These errors have the potential to distort phylogenetic and population clustering analyses, and to mislead tests of admixture using D statistics. We introduce Consensify, a method for generating pseudohaploid sequences, which controls for biases resulting from differential sequencing coverage while greatly reducing error rates. The error correction is derived directly from the data itself, without the requirement for additional genomic resources or simplifying assumptions such as contemporaneous sampling. For phylogenetic and population clustering analysis, we find that Consensify is less affected by artefacts than methods based on single read sampling. For D statistics, Consensify is more resistant to false positives and appears to be less affected by biases resulting from different laboratory protocols than other frequently used methods. Although Consensify is developed with palaeogenomic data in mind, it is applicable for any low to medium coverage short read datasets. We predict that Consensify will be a useful tool for future studies of palaeogenomes.
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http://dx.doi.org/10.3390/genes11010050DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7017230PMC
January 2020

Molecular identification of late and terminal Pleistocene Equus ovodovi from northeastern China.

PLoS One 2019 16;14(5):e0216883. Epub 2019 May 16.

State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan, China.

The extant diversity of horses (family Equidae) represents a small fraction of that occurring over their evolutionary history. One such lost lineage is the subgenus Sussemionus, which is thought to have become extinct during the Middle Pleistocene. However, recent molecular studies and morphological analysis have revealed that one of their representatives, E. ovodovi, did exist in Siberia during the Late Pleistocene. Fossil materials of E. ovodovi have thus far only been found in Russia. In this study, we extracted DNA from three equid fossil specimens excavated from northeastern China dated at 12,770-12,596, 29,525-28,887 and 40,201-38,848 cal. yBP, respectively, and retrieved three near-complete mitochondrial genomes from the specimens. Phylogenetic analyses cluster the Chinese haplotypes together with previously published Russian E. ovodovi, strongly supporting the assignment of these samples to this taxon. The molecular identification of E. ovodovi in northeastern China extends the known geographical range of this fossil species by several thousand kilometers to the east. The estimated coalescence time of all E. ovodovi haplotypes is approximately 199 Kya, with the Chinese haplotypes coalescing approximately 130 Kya. With a radiocarbon age of 12,770-12,596 cal. yBP, the youngest sample in this study represents the first E. ovodovi sample dating to the terminal Pleistocene, moving the extinction date of this species forwards considerably compared to previously documented fossils. Overall, comparison of our three mitochondrial genomes with the two published ones suggests a genetic diversity similar to several extant species of the genus Equus.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0216883PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6522033PMC
January 2020

Paleogenome Reveals Genetic Contribution of Extinct Giant Panda to Extant Populations.

Curr Biol 2019 05 9;29(10):1695-1700.e6. Epub 2019 May 9.

Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, 14476 Potsdam, Germany. Electronic address:

Historically, the giant panda was widely distributed from northern China to southwestern Asia [1]. As a result of range contraction and fragmentation, extant individuals are currently restricted to fragmented mountain ranges on the eastern margin of the Qinghai-Tibet plateau, where they are distributed among three major population clusters [2]. However, little is known about the genetic consequences of this dramatic range contraction. For example, were regions where giant pandas previously existed occupied by ancestors of present-day populations, or were these regions occupied by genetically distinct populations that are now extinct? If so, is there any contribution of these extinct populations to the genomes of giant pandas living today? To investigate these questions, we sequenced the nuclear genome of an ∼5,000-year-old giant panda from Jiangdongshan, Tengchong County in Yunnan Province, China. We find that this individual represents a genetically distinct population that diverged prior to the diversification of modern giant panda populations. We find evidence of differential admixture with this ancient population among modern individuals originating from different populations as well as within the same population. We also find evidence for directional gene flow, which transferred alleles from the ancient population into the modern giant panda lineages. A variable proportion of the genomes of extant individuals is therefore likely derived from the ancient population represented by our sequenced individual. Although extant giant panda populations retain reasonable genetic diversity, our results suggest that this represents only part of the genetic diversity this species harbored prior to its recent range contractions.
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http://dx.doi.org/10.1016/j.cub.2019.04.021DOI Listing
May 2019

Double-Stranded Library Preparation for Ancient and Other Degraded Samples.

Methods Mol Biol 2019 ;1963:65-73

Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany.

High-throughput sequencing (HTS) allows fast and cost-efficient sequencing of ancient DNA (aDNA) without prior information about what sequences should be targeted. One necessary step for HTS is the preparation of a sequencing library. Commercial kits are available for this purpose, but many of these are not suitable for aDNA or other types of damaged DNA. Here, we outline a protocol for HTS library preparation that is optimized for ancient DNA. We report the library conversion rate for a range of input template and adapter concentrations. Our results show that the protocol performs at a high efficiency.
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http://dx.doi.org/10.1007/978-1-4939-9176-1_8DOI Listing
September 2019

Historical biogeography of the leopard (Panthera pardus) and its extinct Eurasian populations.

BMC Evol Biol 2018 10 23;18(1):156. Epub 2018 Oct 23.

Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Straße 24-25, 14476, Potsdam, Germany.

Background: Resolving the historical biogeography of the leopard (Panthera pardus) is a complex issue, because patterns inferred from fossils and from molecular data lack congruence. Fossil evidence supports an African origin, and suggests that leopards were already present in Eurasia during the Early Pleistocene. Analysis of DNA sequences however, suggests a more recent, Middle Pleistocene shared ancestry of Asian and African leopards. These contrasting patterns led researchers to propose a two-stage hypothesis of leopard dispersal out of Africa: an initial Early Pleistocene colonisation of Asia and a subsequent replacement by a second colonisation wave during the Middle Pleistocene. The status of Late Pleistocene European leopards within this scenario is unclear: were these populations remnants of the first dispersal, or do the last surviving European leopards share more recent ancestry with their African counterparts?

Results: In this study, we generate and analyse mitogenome sequences from historical samples that span the entire modern leopard distribution, as well as from Late Pleistocene remains. We find a deep bifurcation between African and Eurasian mitochondrial lineages (~ 710 Ka), with the European ancient samples as sister to all Asian lineages (~ 483 Ka). The modern and historical mainland Asian lineages share a relatively recent common ancestor (~ 122 Ka), and we find one Javan sample nested within these.

Conclusions: The phylogenetic placement of the ancient European leopard as sister group to Asian leopards suggests that these populations originate from the same out-of-Africa dispersal which founded the Asian lineages. The coalescence time found for the mitochondrial lineages aligns well with the earliest undisputed fossils in Eurasia, and thus encourages a re-evaluation of the identification of the much older putative leopard fossils from the region. The relatively recent ancestry of all mainland Asian leopard lineages suggests that these populations underwent a severe population bottleneck during the Pleistocene. Finally, although only based on a single sample, the unexpected phylogenetic placement of the Javan leopard could be interpreted as evidence for exchange of mitochondrial lineages between Java and mainland Asia, calling for further investigation into the evolutionary history of this subspecies.
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http://dx.doi.org/10.1186/s12862-018-1268-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6198532PMC
October 2018

Integration of nuclear and mitochondrial gene sequences and morphology reveals unexpected diversity in the forest cobra (Naja melanoleuca) species complex in Central and West Africa (Serpentes: Elapidae).

Zootaxa 2018 Aug 1;4455(1):68-98. Epub 2018 Aug 1.

Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor University, Bangor LL57 2UW, United Kingdom..

Cobras are among the most widely known venomous snakes, and yet their taxonomy remains incompletely understood, particularly in Africa. Here, we use a combination of mitochondrial and nuclear gene sequences and morphological data to diagnose species limits within the African forest cobra, Naja (Boulengerina) melanoleuca. Mitochondrial DNA sequences reveal deep divergences within this taxon. Congruent patterns of variation in mtDNA, nuclear genes and morphology support the recognition of five separate species, confirming the species status of N. subfulva and N. peroescobari, and revealing two previously unnamed West African species, which are described as new: Naja (Boulengerina) guineensis sp. nov. Broadley, Trape, Chirio, Ineich Wüster, from the Upper Guinea forest of West Africa, and Naja (Boulengerina) savannula sp. nov. Broadley, Trape, Chirio Wüster, a banded form from the savanna-forest mosaic of the Guinea and Sudanian savannas of West Africa. The discovery of cryptic diversity in this iconic group highlights our limited understanding of tropical African biodiversity, hindering our ability to conserve it effectively.
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http://dx.doi.org/10.11646/zootaxa.4455.1.3DOI Listing
August 2018

Partial genomic survival of cave bears in living brown bears.

Nat Ecol Evol 2018 10 27;2(10):1563-1570. Epub 2018 Aug 27.

Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany.

Although many large mammal species went extinct at the end of the Pleistocene epoch, their DNA may persist due to past episodes of interspecies admixture. However, direct empirical evidence of the persistence of ancient alleles remains scarce. Here, we present multifold coverage genomic data from four Late Pleistocene cave bears (Ursus spelaeus complex) and show that cave bears hybridized with brown bears (Ursus arctos) during the Pleistocene. We develop an approach to assess both the directionality and relative timing of gene flow. We find that segments of cave bear DNA still persist in the genomes of living brown bears, with cave bears contributing 0.9 to 2.4% of the genomes of all brown bears investigated. Our results show that even though extinction is typically considered as absolute, following admixture, fragments of the gene pool of extinct species can survive for tens of thousands of years in the genomes of extant recipient species.
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http://dx.doi.org/10.1038/s41559-018-0654-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6590514PMC
October 2018

Multilocus phylogeny, species age and biogeography of the Lesser Antillean anoles.

Mol Phylogenet Evol 2018 10 22;127:682-695. Epub 2018 Jun 22.

School of Biological Sciences, College of Natural Sciences, Bangor University, Deiniol Road, Bangor LL57 2UW, UK.

Lesser Antillean anoles provide classic examples of island radiations. A detailed knowledge of their phylogeny and biogeography, in particular how the age of species relate to the ages of their respective islands and the age of their radiation, is essential to elucidate the tempo and mechanisms of these radiations. We conduct a large-scale phylogenetic and phylogeographic investigation of the Lesser Antillean anoles using multiple genetic markers and comprehensive geographic sampling of most species. The multilocus phylogeny gives the first well-supported reconstruction of the interspecific relationships, and the densely sampled phylogeography reveals a highly dynamic system, driven by overseas dispersal, with several alternative post-dispersal colonisation trajectories. These radiations currently occupy both the outer-older (Eocene to Miocene), and the inner-younger (<8mybp), Lesser Antillean arcs. The origin of these radiations corresponds with the age of the ancient outer arc. However, the ages of extant species (compatible with the age of other small terrestrial amniotes) are much younger, about the age of the emergence of the younger arc, or less. The difference between the age of the radiation and the age of the extant species suggests substantial species turnover on older arc islands, most likely through competitive replacement. Although extant anoles are extremely speciose, this may represent only a fraction of their biodiversity over time. While paraphyly enables us to infer several recent colonization events, the absence of the younger arc islands and extant species at the earlier and middle stages of the radiation, does not allow the earlier inter-island colonization to be reliably inferred. Reproductive isolation in allopatry takes a very considerable time (in excess of 8my) and sympatry appears to occur only late in the radiation. The resolved multilocus phylogeny, and relative species age, raise difficulties for some earlier hypotheses regarding size evolution, and provide no evidence for within-island speciation.
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http://dx.doi.org/10.1016/j.ympev.2018.06.014DOI Listing
October 2018

Optimized DNA sampling of ancient bones using Computed Tomography scans.

Mol Ecol Resour 2018 Nov 27;18(6):1196-1208. Epub 2018 Jun 27.

Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany.

The prevalence of contaminant microbial DNA in ancient bone samples represents the principal limiting factor for palaeogenomic studies, as it may comprise more than 99% of DNA molecules obtained. Efforts to exclude or reduce this contaminant fraction have been numerous but also variable in their success. Here, we present a simple but highly effective method to increase the relative proportion of endogenous molecules obtained from ancient bones. Using computed tomography (CT) scanning, we identify the densest region of a bone as optimal for sampling. This approach accurately identifies the densest internal regions of petrous bones, which are known to be a source of high-purity ancient DNA. For ancient long bones, CT scans reveal a high-density outermost layer, which has been routinely removed and discarded prior to DNA extraction. For almost all long bones investigated, we find that targeted sampling of this outermost layer provides an increase in endogenous DNA content over that obtained from softer, trabecular bone. This targeted sampling can produce as much as 50-fold increase in the proportion of endogenous DNA, providing a directly proportional reduction in sequencing costs for shotgun sequencing experiments. The observed increases in endogenous DNA proportion are not associated with any reduction in absolute endogenous molecule recovery. Although sampling the outermost layer can result in higher levels of human contamination, some bones were found to have more contamination associated with the internal bone structures. Our method is highly consistent, reproducible and applicable across a wide range of bone types, ages and species. We predict that this discovery will greatly extend the potential to study ancient populations and species in the genomics era.
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http://dx.doi.org/10.1111/1755-0998.12911DOI Listing
November 2018

Ancient DNA from Giant Panda (Ailuropoda melanoleuca) of South-Western China Reveals Genetic Diversity Loss during the Holocene.

Genes (Basel) 2018 Apr 6;9(4). Epub 2018 Apr 6.

State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China.

The giant panda was widely distributed in China and south-eastern Asia during the middle to late Pleistocene, prior to its habitat becoming rapidly reduced in the Holocene. While conservation reserves have been established and population numbers of the giant panda have recently increased, the interpretation of its genetic diversity remains controversial. Previous analyses, surprisingly, have indicated relatively high levels of genetic diversity raising issues concerning the efficiency and usefulness of reintroducing individuals from captive populations. However, due to a lack of DNA data from fossil specimens, it is unknown whether genetic diversity was even higher prior to the most recent population decline. We amplified complete cyt and 12s rRNA, partial 16s rRNA and , and control region sequences from the mitochondrial genomes of two Holocene panda specimens. We estimated genetic diversity and population demography by analyzing the ancient mitochondrial DNA sequences alongside those from modern giant pandas, as well as from other members of the bear family (Ursidae). Phylogenetic analyses show that one of the ancient haplotypes is sister to all sampled modern pandas and the second ancient individual is nested among the modern haplotypes, suggesting that genetic diversity may indeed have been higher earlier during the Holocene. Bayesian skyline plot analysis supports this view and indicates a slight decline in female effective population size starting around 6000 years B.P., followed by a recovery around 2000 years ago. Therefore, while the genetic diversity of the giant panda has been affected by recent habitat contraction, it still harbors substantial genetic diversity. Moreover, while its still low population numbers require continued conservation efforts, there seem to be no immediate threats from the perspective of genetic evolutionary potential.
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http://dx.doi.org/10.3390/genes9040198DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5924540PMC
April 2018

Testing of Alignment Parameters for Ancient Samples: Evaluating and Optimizing Mapping Parameters for Ancient Samples Using the TAPAS Tool.

Genes (Basel) 2018 Mar 13;9(3). Epub 2018 Mar 13.

Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476 Potsdam, Germany.

High-throughput sequence data retrieved from ancient or other degraded samples has led to unprecedented insights into the evolutionary history of many species, but the analysis of such sequences also poses specific computational challenges. The most commonly used approach involves mapping sequence reads to a reference genome. However, this process becomes increasingly challenging with an elevated genetic distance between target and reference or with the presence of contaminant sequences with high sequence similarity to the target species. The evaluation and testing of mapping efficiency and stringency are thus paramount for the reliable identification and analysis of ancient sequences. In this paper, we present 'TAPAS', (Testing of Alignment Parameters for Ancient Samples), a computational tool that enables the systematic testing of mapping tools for ancient data by simulating sequence data reflecting the properties of an ancient dataset and performing test runs using the mapping software and parameter settings of interest. We showcase TAPAS by using it to assess and improve mapping strategy for a degraded sample from a banded linsang (), for which no closely related reference is currently available. This enables a 1.8-fold increase of the number of mapped reads without sacrificing mapping specificity. The increase of mapped reads effectively reduces the need for additional sequencing, thus making more economical use of time, resources, and sample material.
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http://dx.doi.org/10.3390/genes9030157DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5867878PMC
March 2018

Extended and Continuous Decline in Effective Population Size Results in Low Genomic Diversity in the World's Rarest Hyena Species, the Brown Hyena.

Mol Biol Evol 2018 05;35(5):1225-1237

Evolutionary Adaptive Genomics, Institute of Biochemistry and Biology, University of Potsdam, Potsdam, Germany.

Hyenas (family Hyaenidae), as the sister group to cats (family Felidae), represent a deeply diverging branch within the cat-like carnivores (Feliformia). With an estimated population size of <10,000 individuals worldwide, the brown hyena (Parahyaena brunnea) represents the rarest of the four extant hyena species and has been listed as Near Threatened by the IUCN. Here, we report a high-coverage genome from a captive bred brown hyena and both mitochondrial and low-coverage nuclear genomes of 14 wild-caught brown hyena individuals from across southern Africa. We find that brown hyena harbor extremely low genetic diversity on both the mitochondrial and nuclear level, most likely resulting from a continuous and ongoing decline in effective population size that started ∼1 Ma and dramatically accelerated towards the end of the Pleistocene. Despite the strikingly low genetic diversity, we find no evidence of inbreeding within the captive bred individual and reveal phylogeographic structure, suggesting the existence of several potential subpopulations within the species.
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http://dx.doi.org/10.1093/molbev/msy037DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5913678PMC
May 2018

Reduction of the contaminant fraction of DNA obtained from an ancient giant panda bone.

BMC Res Notes 2017 Dec 20;10(1):754. Epub 2017 Dec 20.

Faculty of Mathematics and Natural Sciences, Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, 14476, Potsdam, Germany.

Objective: A key challenge in ancient DNA research is massive microbial DNA contamination from the deposition site which accumulates post mortem in the study organism's remains. Two simple and cost-effective methods to enrich the relative endogenous fraction of DNA in ancient samples involve treatment of sample powder with either bleach or Proteinase K pre-digestion prior to DNA extraction. Both approaches have yielded promising but varying results in other studies. Here, we contribute data on the performance of these methods using a comprehensive and systematic series of experiments applied to a single ancient bone fragment from a giant panda (Ailuropoda melanoleuca).

Results: Bleach and pre-digestion treatments increased the endogenous DNA content up to ninefold. However, the absolute amount of DNA retrieved was dramatically reduced by all treatments. We also observed reduced DNA damage patterns in pre-treated libraries compared to untreated ones, resulting in longer mean fragment lengths and reduced thymine over-representation at fragment ends. Guanine-cytosine (GC) contents of both mapped and total reads are consistent between treatments and conform to general expectations, indicating no obvious biasing effect of the applied methods. Our results therefore confirm the value of bleach and pre-digestion as tools in palaeogenomic studies, providing sufficient material is available.
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http://dx.doi.org/10.1186/s13104-017-3061-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5738828PMC
December 2017

Evolutionary History of Saber-Toothed Cats Based on Ancient Mitogenomics.

Curr Biol 2017 Nov 19;27(21):3330-3336.e5. Epub 2017 Oct 19.

Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Straße 24-25, 14476 Potsdam, Germany.

Saber-toothed cats (Machairodontinae) are among the most widely recognized representatives of the now largely extinct Pleistocene megafauna. However, many aspects of their ecology, evolution, and extinction remain uncertain. Although ancient-DNA studies have led to huge advances in our knowledge of these aspects of many other megafauna species (e.g., mammoths and cave bears), relatively few ancient-DNA studies have focused on saber-toothed cats [1-3], and they have been restricted to short fragments of mitochondrial DNA. Here we investigate the evolutionary history of two lineages of saber-toothed cats (Smilodon and Homotherium) in relation to living carnivores and find that the Machairodontinae form a well-supported clade that is distinct from all living felids. We present partial mitochondrial genomes from one S. populator sample and three Homotherium sp. samples, including the only Late Pleistocene Homotherium sample from Eurasia [4]. We confirm the identification of the unique Late Pleistocene European fossil through ancient-DNA analyses, thus strengthening the evidence that Homotherium occurred in Europe over 200,000 years later than previously believed. This in turn forces a re-evaluation of its demography and extinction dynamics. Within the Machairodontinae, we find a deep divergence between Smilodon and Homotherium (∼18 million years) but limited diversity between the American and European Homotherium specimens. The genetic data support the hypothesis that all Late Pleistocene (or post-Villafrancian) Homotherium should be considered a single species, H. latidens, which was previously proposed based on morphological data [5, 6].
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http://dx.doi.org/10.1016/j.cub.2017.09.033DOI Listing
November 2017

Plio-Pleistocene phylogeography of the Southeast Asian Blue Panchax killifish, Aplocheilus panchax.

PLoS One 2017 25;12(7):e0179557. Epub 2017 Jul 25.

Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Environment Centre Wales, Bangor University, Bangor, United Kingdom.

The complex climatic and geological history of Southeast Asia has shaped this region's high biodiversity. In particular, sea level fluctuations associated with repeated glacial cycles during the Pleistocene both facilitated, and limited, connectivity between populations. In this study, we used data from two mitochondrial and three anonymous nuclear markers to determine whether a fresh/brackish water killifish, Aplocheilus panchax, Hamilton, 1822, could be used to further understand how climatic oscillations and associated sea level fluctuations have shaped the distribution of biota within this region, and whether such patterns show evidence of isolation within palaeodrainage basins. Our analyses revealed three major mitochondrial clades within A. panchax. The basal divergence of A. panchax mitochondrial lineages was approximately 3.5 Ma, whilst the subsequent divergence timings of these clades occurred early Pleistocene (~2.6 Ma), proceeding through the Pleistocene. Continuous phylogeographic analysis showed a clear west-east dispersal followed by rapid radiation across Southeast Asia. Individuals from Krabi, just north of the Isthmus of Kra, were more closely related to the Indian lineages, providing further evidence for a freshwater faunal disjunction at the Isthmus of Kra biogeographic barrier. Our results suggest that Sulawesi, across the Wallace Line, was colonised relatively recently (~30 ka). Nuclear DNA is less geographically structured, although Mantel tests indicated that nuclear genetic distances were correlated with geographic proximity. Overall, these results imply that recent gene flow, as opposed to historical isolation, has been the key factor determining patterns of nuclear genetic variation in A. panchax, however, some evidence of historical isolation is retained within the mitochondrial genome. Our study further validates the existence of a major biogeographic boundary at the Kra Isthmus, and also demonstrates the use of widely distributed fresh/brackishwater species in phylogeographic studies, and their ability to disperse across major marine barriers in relatively recent time periods.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0179557PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5526567PMC
September 2017

A mitogenomic timetree for Darwin's enigmatic South American mammal Macrauchenia patachonica.

Nat Commun 2017 06 27;8:15951. Epub 2017 Jun 27.

University of Potsdam, Institute of Biochemistry and Biology, Karl-Liebknecht-Str. 24-25, 14476 Potsdam, Germany.

The unusual mix of morphological traits displayed by extinct South American native ungulates (SANUs) confounded both Charles Darwin, who first discovered them, and Richard Owen, who tried to resolve their relationships. Here we report an almost complete mitochondrial genome for the litoptern Macrauchenia. Our dated phylogenetic tree places Macrauchenia as sister to Perissodactyla, but close to the radiation of major lineages within Laurasiatheria. This position is consistent with a divergence estimate of ∼66 Ma (95% credibility interval, 56.64-77.83 Ma) obtained for the split between Macrauchenia and other Panperissodactyla. Combined with their morphological distinctiveness, this evidence supports the positioning of Litopterna (possibly in company with other SANU groups) as a separate order within Laurasiatheria. We also show that, when using strict criteria, extinct taxa marked by deep divergence times and a lack of close living relatives may still be amenable to palaeogenomic analysis through iterative mapping against more distant relatives.
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http://dx.doi.org/10.1038/ncomms15951DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5490259PMC
June 2017

Tropical ancient DNA reveals relationships of the extinct Bahamian giant tortoise Chelonoidis alburyorum.

Proc Biol Sci 2017 01;284(1846)

Museum of Zoology, Senckenberg Dresden, A. B. Meyer Building, 01109 Dresden, Germany

Ancient DNA of extinct species from the Pleistocene and Holocene has provided valuable evolutionary insights. However, these are largely restricted to mammals and high latitudes because DNA preservation in warm climates is typically poor. In the tropics and subtropics, non-avian reptiles constitute a significant part of the fauna and little is known about the genetics of the many extinct reptiles from tropical islands. We have reconstructed the near-complete mitochondrial genome of an extinct giant tortoise from the Bahamas (Chelonoidis alburyorum) using an approximately 1 000-year-old humerus from a water-filled sinkhole (blue hole) on Great Abaco Island. Phylogenetic and molecular clock analyses place this extinct species as closely related to Galápagos (C. niger complex) and Chaco tortoises (C. chilensis), and provide evidence for repeated overseas dispersal in this tortoise group. The ancestors of extant Chelonoidis species arrived in South America from Africa only after the opening of the Atlantic Ocean and dispersed from there to the Caribbean and the Galápagos Islands. Our results also suggest that the anoxic, thermally buffered environment of blue holes may enhance DNA preservation, and thus are opening a window for better understanding evolution and population history of extinct tropical species, which would likely still exist without human impact.
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http://dx.doi.org/10.1098/rspb.2016.2235DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5247498PMC
January 2017

Complex Admixture Preceded and Followed the Extinction of Wisent in the Wild.

Mol Biol Evol 2017 03;34(3):598-612

Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany.

Retracing complex population processes that precede extreme bottlenecks may be impossible using data from living individuals. The wisent (Bison bonasus), Europe's largest terrestrial mammal, exemplifies such a population history, having gone extinct in the wild but subsequently restored by captive breeding efforts. Using low coverage genomic data from modern and historical individuals, we investigate population processes occurring before and after this extinction. Analysis of aligned genomes supports the division of wisent into two previously recognized subspecies, but almost half of the genomic alignment contradicts this population history as a result of incomplete lineage sorting and admixture. Admixture between subspecies populations occurred prior to extinction and subsequently during the captive breeding program. Admixture with the Bos cattle lineage is also widespread but results from ancient events rather than recent hybridization with domestics. Our study demonstrates the huge potential of historical genomes for both studying evolutionary histories and for guiding conservation strategies.
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http://dx.doi.org/10.1093/molbev/msw254DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5356474PMC
March 2017

Multi-locus phylogeny and species delimitation of Australo-Papuan blacksnakes (Pseudechis Wagler, 1830: Elapidae: Serpentes).

Mol Phylogenet Evol 2017 02 13;107:48-55. Epub 2016 Sep 13.

School of Biological Sciences, Environment Centre Wales, Bangor University, Bangor LL57 2UW, United Kingdom.

Genetic analyses of Australasian organisms have resulted in the identification of extensive cryptic diversity across the continent. The venomous elapid snakes are among the best-studied organismal groups in this region, but many knowledge gaps persist: for instance, despite their iconic status, the species-level diversity among Australo-Papuan blacksnakes (Pseudechis) has remained poorly understood due to the existence of a group of cryptic species within the P. australis species complex, collectively termed "pygmy mulga snakes". Using two mitochondrial and three nuclear loci we assess species boundaries within the genus using Bayesian species delimitation methods and reconstruct their phylogenetic history using multispecies coalescent approaches. Our analyses support the recognition of 10 species, including all of the currently described pygmy mulga snakes and one undescribed species from the Northern Territory of Australia. Phylogenetic relationships within the genus are broadly consistent with previous work, with the recognition of three major groups, the viviparous red-bellied black snake P. porphyriacus forming the sister species to two clades consisting of ovoviviparous species.
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http://dx.doi.org/10.1016/j.ympev.2016.09.005DOI Listing
February 2017

Ancient DNA reveals differences in behaviour and sociality between brown bears and extinct cave bears.

Mol Ecol 2016 10 6;25(19):4907-18. Epub 2016 Sep 6.

Institute for Biochemistry and Biology, University of Potsdam, 14476, Potsdam OT Golm, Germany.

Ancient DNA studies have revolutionized the study of extinct species and populations, providing insights on phylogeny, phylogeography, admixture and demographic history. However, inferences on behaviour and sociality have been far less frequent. Here, we investigate the complete mitochondrial genomes of extinct Late Pleistocene cave bears and middle Holocene brown bears that each inhabited multiple geographically proximate caves in northern Spain. In cave bears, we find that, although most caves were occupied simultaneously, each cave almost exclusively contains a unique lineage of closely related haplotypes. This remarkable pattern suggests extreme fidelity to their birth site in cave bears, best described as homing behaviour, and that cave bears formed stable maternal social groups at least for hibernation. In contrast, brown bears do not show any strong association of mitochondrial lineage and cave, suggesting that these two closely related species differed in aspects of their behaviour and sociality. This difference is likely to have contributed to cave bear extinction, which occurred at a time in which competition for caves between bears and humans was likely intense and the ability to rapidly colonize new hibernation sites would have been crucial for the survival of a species so dependent on caves for hibernation as cave bears. Our study demonstrates the potential of ancient DNA to uncover patterns of behaviour and sociality in ancient species and populations, even those that went extinct many tens of thousands of years ago.
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http://dx.doi.org/10.1111/mec.13800DOI Listing
October 2016

Is Hybridization a Source of Adaptive Venom Variation in Rattlesnakes? A Test, Using a Crotalus scutulatus × viridis Hybrid Zone in Southwestern New Mexico.

Toxins (Basel) 2016 06 16;8(6). Epub 2016 Jun 16.

Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK.

Venomous snakes often display extensive variation in venom composition both between and within species. However, the mechanisms underlying the distribution of different toxins and venom types among populations and taxa remain insufficiently known. Rattlesnakes (Crotalus, Sistrurus) display extreme inter- and intraspecific variation in venom composition, centered particularly on the presence or absence of presynaptically neurotoxic phospholipases A₂ such as Mojave toxin (MTX). Interspecific hybridization has been invoked as a mechanism to explain the distribution of these toxins across rattlesnakes, with the implicit assumption that they are adaptively advantageous. Here, we test the potential of adaptive hybridization as a mechanism for venom evolution by assessing the distribution of genes encoding the acidic and basic subunits of Mojave toxin across a hybrid zone between MTX-positive Crotalus scutulatus and MTX-negative C. viridis in southwestern New Mexico, USA. Analyses of morphology, mitochondrial and single copy-nuclear genes document extensive admixture within a narrow hybrid zone. The genes encoding the two MTX subunits are strictly linked, and found in most hybrids and backcrossed individuals, but not in C. viridis away from the hybrid zone. Presence of the genes is invariably associated with presence of the corresponding toxin in the venom. We conclude that introgression of highly lethal neurotoxins through hybridization is not necessarily favored by natural selection in rattlesnakes, and that even extensive hybridization may not lead to introgression of these genes into another species.
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http://dx.doi.org/10.3390/toxins8060188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4926154PMC
June 2016

Widespread parallel population adaptation to climate variation across a radiation: implications for adaptation to climate change.

Mol Ecol 2015 Mar 16;24(5):1019-30. Epub 2015 Feb 16.

School of Biological Sciences, Bangor University, ECW Building, Bangor, Gwynedd, LL57 2UW, UK.

Global warming will impact species in a number of ways, and it is important to know the extent to which natural populations can adapt to anthropogenic climate change by natural selection. Parallel microevolution within separate species can demonstrate natural selection, but several studies of homoplasy have not yet revealed examples of widespread parallel evolution in a generic radiation. Taking into account primary phylogeographic divisions, we investigate numerous quantitative traits (size, shape, scalation, colour pattern and hue) in anole radiations from the mountainous Lesser Antillean islands. Adaptation to climatic differences can lead to very pronounced differences between spatially close populations with all studied traits showing some evidence of parallel evolution. Traits from shape, scalation, pattern and hue (particularly the latter) show widespread evolutionary parallels within these species in response to altitudinal climate variation greater than extreme anthropogenic climate change predicted for 2080. This gives strong evidence of the ability to adapt to climate variation by natural selection throughout this radiation. As anoles can evolve very rapidly, it suggests anthropogenic climate change is likely to be less of a conservation threat than other factors, such as habitat loss and invasive species, in this, Lesser Antillean, biodiversity hot spot.
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http://dx.doi.org/10.1111/mec.13093DOI Listing
March 2015

The future of ancient DNA: Technical advances and conceptual shifts.

Bioessays 2015 Mar 21;37(3):284-93. Epub 2014 Nov 21.

Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany; Department of Biology, University of York, York, UK.

Technological innovations such as next generation sequencing and DNA hybridisation enrichment have resulted in multi-fold increases in both the quantity of ancient DNA sequence data and the time depth for DNA retrieval. To date, over 30 ancient genomes have been sequenced, moving from 0.7× coverage (mammoth) in 2008 to more than 50× coverage (Neanderthal) in 2014. Studies of rapid evolutionary changes, such as the evolution and spread of pathogens and the genetic responses of hosts, or the genetics of domestication and climatic adaptation, are developing swiftly and the importance of palaeogenomics for investigating evolutionary processes during the last million years is likely to increase considerably. However, these new datasets require new methods of data processing and analysis, as well as conceptual changes in interpreting the results. In this review we highlight important areas of future technical and conceptual progress and discuss research topics in the rapidly growing field of palaeogenomics.
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http://dx.doi.org/10.1002/bies.201400160DOI Listing
March 2015