Eleftheria Palkopoulou

Serial population extinctions in a small mammal indicate Late Pleistocene ecosystem instability

The Late Pleistocene global extinction of many terrestrial mammal species has been a subject of intensive scientific study for over a century, yet the relative contributions of environmental changes and the global expansion of humans remain unresolved. A defining component of these extinctions is a bias toward large species, with the majority of small-mammal taxa apparently surviving into the present. Here, we investigate the population-level history of a key tundra-specialist small mammal, the collared lemming (Dicrostonyx torquatus), to explore whether events during the Late Pleistocene had a discernible effect beyond the large mammal fauna. Using ancient DNA techniques to sample across three sites in North-West Europe, we observe a dramatic reduction in genetic diversity in this species over the last 50,000 y. We further identify a series of extinction-recolonization events, indicating a previously unrecognized instability in Late Pleistocene small-mammal populations, which we link with climatic fluctuations. Our results reveal climate-associated, repeated regional extinctions in a keystone prey species across the Late Pleistocene, a pattern likely to have had an impact on the wider steppe-tundra community, and one that is concordant with environmental change as a major force in structuring Late Pleistocene biodiversity.

Holarctic genetic structure and range dynamics in the woolly mammoth

Ancient DNA analyses have provided enhanced resolution of population histories in many Pleistocene taxa. However, most studies are spatially restricted, making inference of species-level biogeographic histories difficult. Here, we analyse mitochondrial DNA (mtDNA) variation in the woolly mammoth from across its Holarctic range to reconstruct its history over the last 200 thousand years (kyr). We identify a previously undocumented major mtDNA lineage in Europe, which was replaced by another major mtDNA lineage 32–34 kyr before present (BP). Coalescent simulations provide support for demographic expansions at approximately 121 kyr BP, suggesting that the previous interglacial was an important driver for demography and intraspecific genetic divergence. Furthermore, our results suggest an expansion into Eurasia from America around 66 kyr BP, coinciding with the first exposure of the Bering Land Bridge during the Late Pleistocene. Bayesian inference indicates Late Pleistocene demographic stability until 20–15 kyr BP, when a severe population size decline occurred.

Population structure and recent temporal changes in genetic variation in Eurasian otters from Sweden

The Eurasian otter (Lutra lutra) population in Sweden went through a drastic decline in population size between the 1950s and 1980s, caused mostly by anthropogenic factors such as high hunting pressure and the introduction of environmental toxic chemicals into the otter’s habitats. However, after the bans of PCBs and DDT in the 1970s, the population began to recover in the 1990s. This study compares microsatellite data across twelve loci from historical and contemporary otter samples to investigate whether there has been a change in population structure and genetic diversity across time in various locations throughout Sweden. The results suggest that otters in the south were more severely affected by the bottleneck, demonstrated by a decline in genetic diversity and a shift in genetic composition. In contrast, the genetic composition in otters from northern Sweden remained mostly unchanged, both in terms of population structure and diversity. This suggests that the decline was not uniform across the country. Moreover, our analyses of historical samples provide an overview of the level of genetic variation and population structure that existed prior to the bottleneck, which may be helpful for the future management and conservation of the species.

Back to BaySICS: A User-Friendly Program for Bayesian Statistical Inference from Coalescent Simulations

Inference of population demographic history has vastly improved in recent years due to a number of technological and theoretical advances including the use of ancient DNA. Approximate Bayesian computation (ABC) stands among the most promising methods due to its simple theoretical fundament and exceptional flexibility. However, limited availability of user-friendly programs that perform ABC analysis renders it difficult to implement, and hence programming skills are frequently required. In addition, there is limited availability of programs able to deal with heterochronous data. Here we present the software BaySICS: Bayesian Statistical Inference of Coalescent Simulations. BaySICS provides an integrated and user-friendly platform that performs ABC analyses by means of coalescent simulations from DNA sequence data. It estimates historical demographic population parameters and performs hypothesis testing by means of Bayes factors obtained from model comparisons. Although providing specific features that improve inference from datasets with heterochronous data, BaySICS also has several capabilities making it a suitable tool for analysing contemporary genetic datasets. Those capabilities include joint analysis of independent tables, a graphical interface and the implementation of Markov-chain Monte Carlo without likelihoods.

A comprehensive genomic history of extinct and living elephants

Significance Elephantids were once among the most widespread megafaunal families. However, only three species of this family exist today. To reconstruct their evolutionary history, we generated 14 genomes from living and extinct elephantids and from the American mastodon. While previous studies examined only simple bifurcating relationships, we found that gene flow between elephantid species was common in the past. Straight-tusked elephants descend from a mixture of three ancestral populations related to the ancestor of African elephants, woolly mammoths, and present-day forest elephants. We detected interbreeding between North American woolly and Columbian mammoths but found no evidence of recent gene flow between forest and savanna elephants, demonstrating that both gene flow and isolation have been central in the evolution of elephantids. Elephantids are the world’s most iconic megafaunal family, yet there is no comprehensive genomic assessment of their relationships. We report a total of 14 genomes, including 2 from the American mastodon, which is an extinct elephantid relative, and 12 spanning all three extant and three extinct elephantid species including an ∼120,000-y-old straight-tusked elephant, a Columbian mammoth, and woolly mammoths. Earlier genetic studies modeled elephantid evolution via simple bifurcating trees, but here we show that interspecies hybridization has been a recurrent feature of elephantid evolution. We found that the genetic makeup of the straight-tusked elephant, previously placed as a sister group to African forest elephants based on lower coverage data, in fact comprises three major components. Most of the straight-tusked elephant’s ancestry derives from a lineage related to the ancestor of African elephants while its remaining ancestry consists of a large contribution from a lineage related to forest elephants and another related to mammoths. Columbian and woolly mammoths also showed evidence of interbreeding, likely following a latitudinal cline across North America. While hybridization events have shaped elephantid history in profound ways, isolation also appears to have played an important role. Our data reveal nearly complete isolation between the ancestors of the African forest and savanna elephants for ∼500,000 y, providing compelling justification for the conservation of forest and savanna elephants as separate species.

Palaeogenomes of Eurasian straight-tusked elephants challenge the current view of elephant evolution

The straight-tusked elephants Palaeoloxodon spp. were widespread across Eurasia during the Pleistocene. Phylogenetic reconstructions using morphological traits have grouped them with Asian elephants (Elephas maximus), and many paleontologists place Palaeoloxodon within Elephas. Here, we report the recovery of full mitochondrial genomes from four and partial nuclear genomes from two P. antiquus fossils. These fossils were collected at two sites in Germany, Neumark-Nord and Weimar-Ehringsdorf, and likely date to interglacial periods ~120 and ~244 thousand years ago, respectively. Unexpectedly, nuclear and mitochondrial DNA analyses suggest that P. antiquus was a close relative of extant African forest elephants (Loxodonta cyclotis). Species previously referred to Palaeoloxodon are thus most parsimoniously explained as having diverged from the lineage of Loxodonta, indicating that Loxodonta has not been constrained to Africa. Our results demonstrate that the current picture of elephant evolution is in need of substantial revision. DOI: http://dx.doi.org/10.7554/eLife.25413.001

Genetic signs of multiple colonization events in Baltic ciscoes with radiation into sympatric spring- and autumn-spawners confined to early postglacial arrival

Presence of sympatric populations may reflect local diversification or secondary contact of already distinct forms. The Baltic cisco (Coregonus albula) normally spawns in late autumn, but in a few lakes in Northern Europe sympatric autumn and spring- or winter-spawners have been described. So far, the evolutionary relationships and taxonomic status of these main life history forms have remained largely unclear. With microsatellites and mtDNA sequences, we analyzed extant and extinct spring- and autumn-spawners from a total of 23 Swedish localities, including sympatric populations. Published sequences from Baltic ciscoes in Germany and Finland, and Coregonus sardinella from North America were also included together with novel mtDNA sequences from Siberian C. sardinella. A clear genetic structure within Sweden was found that included two population assemblages markedly differentiated at microsatellites and apparently fixed for mtDNA haplotypes from two distinct clades. All sympatric Swedish populations belonged to the same assemblage, suggesting parallel evolution of spring-spawning rather than secondary contact. The pattern observed further suggests that postglacial immigration to Northern Europe occurred from at least two different refugia. Previous results showing that mtDNA in Baltic cisco is paraphyletic with respect to North American C. sardinella were confirmed. However, the inclusion of Siberian C. sardinella revealed a more complicated pattern, as these novel haplotypes were found within one of the two main C. albula clades and were clearly distinct from those in North American C. sardinella. The evolutionary history of Northern Hemisphere ciscoes thus seems to be more complex than previously recognized.

Mitogenome evolution in the last surviving woolly mammoth population reveals neutral and functional consequences of small population size

The onset of the Holocene was associated with a global temperature increase, which led to a rise in sea levels and isolation of the last surviving population of woolly mammoths on Wrangel Island. Understanding what happened with the populations genetic diversity at the time of the isolation and during the ensuing 6000 years can help clarify the effects of bottlenecks and subsequent limited population sizes in species approaching extinction. Previous genetic studies have highlighted questions about how the Holocene Wrangel population was established and how the isolation event affected genetic diversity. Here, we generated high‐quality mitogenomes from 21 radiocarbon‐dated woolly mammoths to compare the ancestral large and genetically diverse Late Pleistocene Siberian population and the small Holocene Wrangel population. Our results indicate that mitogenome diversity was reduced to one single haplotype at the time of the isolation, and thus that the Holocene Wrangel Island population was established by a single maternal lineage. Moreover, we show that the ensuing small effective population size coincided with fixation of a nonsynonymous mutation, and a comparative analysis of mutation rates suggests that the evolutionary rate was accelerated in the Holocene population. These results suggest that isolation on Wrangel Island led to an increase in the frequency of deleterious genetic variation, and thus are consistent with the hypothesis that strong genetic drift in small populations leads to purifying selection being less effective in removing deleterious mutations.

Early Pleistocene enamel proteome sequences from Dmanisi resolve Stephanorhinus phylogeny.

Ancient DNA (aDNA) sequencing has enabled unprecedented reconstruction of speciation, migration, and admixture events for extinct taxa1. Outside the permafrost, however, irreversible aDNA post-mortem degradation2 has so far limited aDNA recovery within the ˜0.5 million years (Ma) time range3. Tandem mass spectrometry (MS)-based collagen type I (COL1) sequencing provides direct access to older biomolecular information4, though with limited phylogenetic use. In the absence of molecular evidence, the speciation of several Early and Middle Pleistocene extinct species remain contentious. In this study, we address the phylogenetic relationships of the Eurasian Pleistocene Rhinocerotidae5-7 using ˜1.77 million years (Ma) old dental enamel proteome sequences of a Stephanorhinus specimen from the Dmanisi archaeological site in Georgia (South Caucasus)8. Molecular phylogenetic analyses place the Dmanisi Stephanorhinus as a sister group to the woolly (Coelodonta antiquitatis) and Merck’s rhinoceros (S. kirchbergensis) clade. We show that Coelodonta evolved from an early Stephanorhinus lineage and that this genus includes at least two distinct evolutionary lines. As such, the genus Stephanorhinus is currently paraphyletic and its systematic revision is therefore needed. We demonstrate that Early Pleistocene dental enamel proteome sequencing overcomes the limits of ancient collagen- and aDNA-based phylogenetic inference, and also provides additional information about the sex and taxonomic assignment of the specimens analysed. Dental enamel, the hardest tissue in vertebrates, is highly abundant in the fossil record. Our findings reveal that palaeoproteomic investigation of this material can push biomolecular investigation further back into the Early Pleistocene.