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The Great Hungarian Plain was a crossroads of cultural transformations that have shaped European prehistory. Here we analyse a 5,000-year transect of human genomes, sampled from petrous bones giving consistently excellent endogenous DNA yields, from 13 Hungarian Neolithic, Copper, Bronze and Iron Age burials including two to high (similar to 22x) and seven to similar to 1x coverage, to investigate the impact of these on Europe's genetic landscape. These data suggest genomic shifts with the advent of the Neolithic, Bronze and Iron Ages, with interleaved periods of genome stability. The earliest Neolithic context genome shows a European hunter-gatherer genetic signature and a restricted ancestral population size, suggesting direct contact between cultures after the arrival of the first farmers into Europe. The latest, Iron Age, sample reveals an eastern genomic influence concordant with introduced Steppe burial rites. We observe transition towards lighter pigmentation and surprisingly, no Neolithic presence of lactase persistence.
Ancient genome provides insights into the history of Eurasian lynx in Iberia and Western Europe
(2022)
The Eurasian lynx (Lynx lynx) is one of the most widely distributed felids in the world. However, most of its populations started to decline a few millennia ago. Historical declines have been especially severe in Europe, and particularly in Western Europe, from where the species disappeared in the last few centuries. Here, we analyze the genome of an Eurasian lynx inhabiting the Iberian Peninsula 2500 ya, to gain insights into the phylogeographic position and genetic status of this extinct population. Also, we contextualize previous ancient data in the light of new phylogeographic studies of the species. Our results suggest that the Iberian population is part of an extinct European lineage closely related to the current Carpathian-Baltic lineages. Also, this sample holds the lowest diversity reported for the species so far, and similar to that of the highly endangered Iberian lynx. A combination of historical factors, such as a founder effect while colonizing the peninsula, together with intensified human impacts during the Holocene in the Cantabrian strip, could have led to a genetic impoverishment of the population and precipitated its extinction. Mitogenomic lineages distribution in space and time support the long-term coexistence of several lineages of Eurasian lynx in Western Europe with fluctuating ranges. While mitochondrial sequences related to the lineages currently found in Balkans and Caucasus were predominant during the Pleistocene, those more closely related to the lineage currently distributed in Central Europe prevailed during the Holocene. The use of ancient genomics has proven to be a useful tool to understand the biogeographic pattern of the Eurasian lynx in the past.
Abstract
By combining high-throughput sequencing with target enrichment (‘hybridization capture’), researchers are able to obtain molecular data from genomic regions of interest for projects that are otherwise constrained by sample quality (e.g. degraded and contamination-rich samples) or a lack of a priori sequence information (e.g. studies on nonmodel species). Despite the use of hybridization capture in various fields of research for many years, the impact of enrichment conditions on capture success is not yet thoroughly understood. We evaluated the impact of a key parameter – hybridization temperature – on the capture success of mitochondrial genomes across the carnivoran family Felidae. Capture was carried out for a range of sample types (fresh, archival, ancient) with varying levels of sequence divergence between bait and target (i.e. across a range of species) using pools of individually indexed libraries on Agilent SureSelect™ arrays. Our results suggest that hybridization capture protocols require specific optimization for the sample type that is being investigated. Hybridization temperature affected the proportion of on-target sequences following capture: for degraded samples, we obtained the best results with a hybridization temperature of 65 °C, while a touchdown approach (65 °C down to 50 °C) yielded the best results for fresh samples. Evaluation of capture performance at a regional scale (sliding window approach) revealed no significant improvement in the recovery of DNA fragments with high sequence divergence from the bait at any of the tested hybridization temperatures, suggesting that hybridization temperature may not be the critical parameter for the enrichment of divergent fragments.
Targeted capture coupled with high-throughput sequencing can be used to gain information about nuclear sequence variation at hundreds to thousands of loci. Divergent reference capture makes use of molecular data of one species to enrich target loci in other (related) species. This is particularly valuable for nonmodel organisms, for which often no a priori knowledge exists regarding these loci. Here, we have used targeted capture to obtain data for 809 nuclear coding DNA sequences (CDS) in a nonmodel organism, the Eurasian lynx Lynx lynx, using baits designed with the help of the published genome of a related model organism (the domestic cat Felis catus). Using this approach, we were able to survey intraspecific variation at hundreds of nuclear loci in L. lynx across the species’ European range. A large set of biallelic candidate SNPs was then evaluated using a high-throughput SNP genotyping platform (Fluidigm), which we then reduced to a final 96 SNP-panel based on assay performance and reliability; validation was carried out with 100 additional Eurasian lynx samples not included in the SNP discovery phase. The 96 SNP-panel developed from CDS performed very successfully in the identification of individuals and in population genetic structure inference (including the assignment of individuals to their source population). In keeping with recent studies, our results show that genic SNPs can be valuable for genetic monitoring of wildlife species.
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.
Insights into the geographical origin and phylogeographical patterns of Paradisaea birds-of-paradise
(2022)
Birds-of-paradise represent a textbook example for geographical speciation and sexual selection. Perhaps the most iconic genus is Paradisaea, which is restricted to New Guinea and a few surrounding islands. Although several species concepts have been applied in the past to disentangle the different entities within this genus, no attempt has been made so far to uncover phylogeographical patterns based on a genetic dataset that includes multiple individuals per species. Here, we applied amplicon sequencing for the mitochondrial fragment Cytb for a total of 69 museum specimens representing all seven Paradisaea species described and inferred both phylogenetic relationships and colonization pathways across the island. Our analyses show that the most recent common ancestor of the diverging lineages within Paradisaea probably originated in the Late Miocene in the eastern part of the Central Range and suggest that tectonic processes played a key role in shaping the diversification and distribution of species. All species were recovered as monophyletic, except for those within the apoda-minor-raggiana clade, which comprises the allopatric and parapatric species P. apoda, P. minor and P. raggiana. The comparatively young divergence times, together with possible instances of mitochondrial introgression and incomplete lineage sorting, suggest recent speciation in this clade.
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.
After initial detection of target archival DNA of a 116-year-old syntype specimen of the smooth lantern shark, Etmopterus pusillus, in a single-stranded DNA library, we shotgun-sequenced additional 9 million reads from this same DNA library. Sequencing reads were used for extracting mitochondrial sequence information for analyses of mitochondrial DNA characteristics and reconstruction of the mitochondrial genome. The archival DNA is highly fragmented. A total of 4599 mitochondrial reads were available for the genome reconstruction using an iterative mapping approach. The resulting genome sequence has 12 times coverage and a length of 16 741 bp. All 37 vertebrate mitochondrial loci plus the control region were identified and annotated. The mitochondrial NADH2 gene was subsequently used to place the syntype haplotype in a network comprising multiple E. pusillus samples from various distant localities as well as sequences from a morphological similar species, the shortfin smooth lantern shark Etmopterus joungi. Results confirm the almost global distribution of E. pusillus and suggest E. joungi to be a junior synonym of E. pusillus. As mitochondrial DNA often represents the only available reference information in non-model organisms, this study illustrates the importance of mitochondrial DNA from an aged, wet collection type specimen for taxonomy.
(1) Background:
Adaptive diversification of complex traits plays a pivotal role in the evolution of organismal diversity. In the freshwater snail genus Tylomelania, adaptive radiations were likely promoted by trophic specialization via diversification of their key foraging organ, the radula.
(2) Methods:
To investigate the molecular basis of radula diversification and its contribution to lineage divergence, we used tissue-specific transcriptomes of two sympatric Tylomelania sarasinorum ecomorphs.
(3) Results:
We show that ecomorphs are genetically divergent lineages with habitat-correlated abundances. Sequence divergence and the proportion of highly differentially expressed genes are significantly higher between radula transcriptomes compared to the mantle and foot. However, the same is not true when all differentially expressed genes or only non-synonymous SNPs are considered. Finally, putative homologs of some candidate genes for radula diversification (hh, arx, gbb) were also found to contribute to trophic specialization in cichlids and Darwin's finches.
(4) Conclusions:
Our results are in line with diversifying selection on the radula driving Tylomelania ecomorph divergence and indicate that some molecular pathways may be especially prone to adaptive diversification, even across phylogenetically distant animal groups.
Etmopteridae (lantern sharks) is the most species-rich family of sharks, comprising more than 50 species.
Many species are described from few individuals, and re-collection of specimens is often hindered by the remoteness of their sampling sites.
For taxonomic studies, comparative morphological analysis of type specimens housed in natural history collections has been the main source of evidence.
In contrast, DNA sequence information has rarely been used.
Most lantern shark collection specimens, including the types, were formalin fixed before long-term storage in ethanol solutions.
The DNA damage caused by both fixation and preservation of specimens has excluded these specimens from DNA sequence-based phylogenetic analyses so far.
However, recent advances in the field of ancient DNA have allowed recovery of wet-collection specimen DNA sequence data.
Here we analyse archival mitochondrial DNA sequences, obtained using ancient DNA approaches, of two wet-collection lantern shark paratype specimens, namely Etmopterus litvinovi and E. pycnolepis, for which the type series represent the only known individuals.
Target capture of mitochondrial markers from single-stranded DNA libraries allows for phylogenetic placement of both species.
Our results suggest synonymy of E. benchleyi with E. litvinovi but support the species status of E. pycnolepis. This revised taxonomy is helpful for future conservation and management efforts, as our results indicate a larger distribution range of E. litvinovi. This study further demonstrates the importance of wet-collection type specimens as genetic resource for taxonomic research.
Mitochondrial genomes of Late Pleistocene caballine horses from China belong to a separate clade
(2020)
There were several species of Equus in northern China during the Late Pleistocene, including Equus przewalskii and Equus dalianensis. A number of morphological studies have been carried out on E. przewalskii and E. dalianensis, but their evolutionary history is still unresolved. In this study, we retrieved near-complete mitochondrial genomes from E. dalianensis and E. przewalskii specimens excavated from Late Pleistocene strata in northeastern China. Phylogenetic analyses revealed that caballoid horses were divided into two subclades: the New World and the Old World caballine horse subclades. The Old World caballine horses comprise of two deep phylogenetic lineages, with modern and ancient Equus caballus and modern E. przewalskii forming lineage I, and the individuals in this study together with one Yakut specimen forming lineage II. Our results indicate that Chinese Late Pleistocene caballoid horses showed a closer relationship to other Eurasian caballine horses than that to Pleistocene horses from North America. In addition, phylogenetic analyses suggested a close relationship between E. dalianensis and the Chinese fossil E. przewalskii, in agreement with previous researches based on morphological analyses. Interestingly, E. dalianensis and the fossil E. przewalskii were intermixed rather than split into distinct lineages, suggesting either that gene flow existed between these two species or that morphology-based species assignment of palaeontological specimens is not always correct. Moreover, Bayesian analysis showed that the divergence time between the New World and the Old World caballoid horses was at 1.02 Ma (95% CI: 0.86-1.24 Ma), and the two Old World lineages (I & II) split at 0.88 Ma (95% CI: 0.69-1.13 Ma), which indicates that caballoid horses seem to have evolved into different populations in the Old World soon after they migrated from North America via the Bering Land Bridge. Finally, the TMRCA of E. dalianensis was estimated at 0.20 Ma (95% CI: 0.15-0.28 Ma), and it showed a relative low genetic diversity compared with other Equus species.
The subgenus Laurentomantis in the genus Gephyromantis contains some of the least known amphibian species of Madagascar. The six currently valid nominal species are rainforest frogs known from few individuals, hampering a full understanding of the species diversity of the clade. We assembled data on specimens collected during field surveys over the past 30 years and integrated analysis of mitochondrial and nuclear-encoded genes of 88 individuals, a comprehensive bioacoustic analysis, and morphological comparisons to delimit a minimum of nine species-level lineages in the subgenus. To clarify the identity of the species Gephyromantis malagasius, we applied a target-enrichment approach to a sample of the 110 year old holotype of Microphryne malagasia Methuen and Hewitt, 1913 to assign this specimen to a lineage based on a mitochondrial DNA barcode. The holotype clustered unambiguously with specimens previously named G. ventrimaculatus. Consequently we propose to consider Trachymantis malagasia ventrimaculatus Angel, 1935 as a junior synonym of Gephyromantis malagasius. Due to this redefinition of G. malagasius, no scientific name is available for any of the four deep lineages of frogs previously subsumed under this name, all characterized by red color ventrally on the hindlimbs. These are here formally named as Gephyromantis fiharimpe sp. nov., G. matsilo sp. nov., G. oelkrugi sp. nov., and G. portonae sp. nov. The new species are distinguishable from each other by genetic divergences of >4% uncorrected pairwise distance in a fragment of the 16S rRNA marker and a combination of morphological and bioacoustic characters. Gephyromantis fiharimpe and G. matsilo occur, respectively, at mid-elevations and lower elevations along a wide stretch of Madagascar's eastern rainforest band, while G. oelkrugi and G. portonae appear to be more range-restricted in parts of Madagascar's North East and Northern Central East regions. Open taxonomic questions surround G. horridus, to which we here assign specimens from Montagne d'Ambre and the type locality Nosy Be; and G. ranjomavo, which contains genetically divergent populations from Marojejy, Tsaratanana, and Ampotsidy.
Paleogenomes reveal a complex evolutionary history of late Pleistocene bison in Northeastern China
(2022)
Steppe bison are a typical representative of the Mid-Late Pleistocene steppes of the northern hemisphere.
Despite the abundance of fossil remains, many questions related to their genetic diversity, population structure and dispersal route are still elusive.
Here, we present both near-complete and partial mitochondrial genomes, as well as a partial nuclear genome from fossil bison samples excavated from Late Pleistocene strata in northeastern China.
Maximum-likelihood and Bayesian trees both suggest the bison clade are divided into three maternal haplogroups (A, B and C), and Chinese individuals fall in two of them. Bayesian analysis shows that the split between haplogroup C and the ancestor of haplogroups A and B dates at 326 ky BP (95% HPD: 397-264 ky BP).
In addition, our nuclear phylogenomic tree also supports a basal position for the individual carrying haplogroup C. Admixture analyses suggest that CADG467 (haplogroup C) has a similar genetic structure to steppe bison from Siberia (haplogroup B).
Our new findings indicate that the genetic diversity of Pleistocene bison was probably even higher than previously thought and that northeastern Chinese populations of several mammalian species, including Pleistocene bison, were genetically distinct.
Otter shrew mitogenomes (Afrotheria, Potamogalidae) reconstructed from historical museum skins
(2022)
African otter shrews (Potamogalidae) are Afrotherian mammals adapted to a semi-aquatic lifestyle. Given their rareness, genetic data on otter shrews are limited. By applying laboratory methods tuned for the recovery of archival DNA and an iterative mapping approach, we reconstructed whole mitochondrial genomes of the Giant (Potamogale velox) and Ruwenzori pygmy otter shrew (Micropotamogale ruwenzorii) from historical museum skins. Phylogenetic analyses are consistent with previous reports in recovering a sister relationship between African otter shrews and Malagasy tenrecs. The long branches separating both lineages, however, support their recognition as separate families.