Many wild species have suffered drastic population size declines over the past centuries, which have led to 'genomic erosion' processes characterized by reduced genetic diversity, increased ...inbreeding, and accumulation of harmful mutations. Yet, genomic erosion estimates of modern-day populations often lack concordance with dwindling population sizes and conservation status of threatened species. One way to directly quantify the genomic consequences of population declines is to compare genome-wide data from pre-decline museum samples and modern samples. However, doing so requires computational data processing and analysis tools specifically adapted to comparative analyses of degraded, ancient or historical, DNA data with modern DNA data as well as personnel trained to perform such analyses.
Here, we present a highly flexible, scalable, and modular pipeline to compare patterns of genomic erosion using samples from disparate time periods. The GenErode pipeline uses state-of-the-art bioinformatics tools to simultaneously process whole-genome re-sequencing data from ancient/historical and modern samples, and to produce comparable estimates of several genomic erosion indices. No programming knowledge is required to run the pipeline and all bioinformatic steps are well-documented, making the pipeline accessible to users with different backgrounds. GenErode is written in Snakemake and Python3 and uses Conda and Singularity containers to achieve reproducibility on high-performance compute clusters. The source code is freely available on GitHub ( https://github.com/NBISweden/GenErode ).
GenErode is a user-friendly and reproducible pipeline that enables the standardization of genomic erosion indices from temporally sampled whole genome re-sequencing data.
Understanding the micro-Âevolutionary response of populations to demographic declines is a major goal in evolutionary and conservation biology. In small populations, genetic drift can lead to an ...accumulation of deleterious mutations, which will increase the risk of extinction. However, demographic recovery can still occur after extreme declines, suggesting that natural selection may purge deleterious mutations, even in extremely small populations. The Chatham Island black robin (Petroica traversi) is arguably the most inbred bird species in the world. It avoided imminent extinction in the early 1980s and after a remarkable recovery from a single pair, a second population was established and the two extant populations have evolved in complete isolation since then. Here, we analysed 52 modern and historical genomes to examine the genomic consequences of this extreme bottleneck and the subsequent translocation. We found evidence for two-fold decline in heterozygosity and three- to four-fold increase in inbreeding in modern genomes. Moreover, there was partial support for temporal reduction in total load for detrimental variation. In contrast, compared to historical genomes, modern genomes showed a significantly higher realised load, reflecting the temporal increase in inbreeding. Furthermore, the translocation induced only small changes in the frequency of deleterious alleles, with the majority of detrimental variation being shared between the two populations. Our results highlight the dynamics of mutational load in a species that recovered from the brink of extinction, and show rather limited temporal changes in mutational load. We hypothesise that ancestral purging may have been facilitated by population fragmentation and isolation on several islands for thousands of generations and may have already reduced much of the highly deleterious load well before human arrival and introduction of pests to the archipelago. The majority of fixed deleterious variation was shared between the modern populations, but translocation of individuals with low mutational load could possibly mitigate further fixation of high-frequency deleterious variation.
Climate warming at the end of the last glacial period had profound effects on the distribution of cold-adapted species. As their range shifted towards northern latitudes, they were able to colonise ...previously glaciated areas, including remote Arctic islands. However, there is still uncertainty about the routes and timing of colonisation. At the end of the last ice age, reindeer/caribou (Rangifer tarandus) expanded to the Holarctic region and colonised the archipelagos of Svalbard and Franz Josef Land. Earlier studies have proposed two possible colonisation routes, either from the Eurasian mainland or from Canada via Greenland. Here, we used 174 ancient, historical and modern mitogenomes to reconstruct the phylogeny of reindeer across its whole range and to infer the colonisation route of the Arctic islands. Our data shows a close affinity among Svalbard, Franz Josef Land and Novaya Zemlya reindeer. We also found tentative evidence for positive selection in the mitochondrial gene ND4, which is possibly associated with increased heat production. Our results thus support a colonisation of the Eurasian Arctic archipelagos from the Eurasian mainland and provide some insights into the evolutionary history and adaptation of the species to its High Arctic habitat.
Starting four decades ago, studies have examined the ecology and evolutionary dynamics of populations and species using short mitochondrial DNA fragments and stable isotopes. Through technological ...and analytical advances, the methods and biomolecules at our disposal have increased significantly to now include lipids, whole genomes, proteomes, and even epigenomes. At an unprecedented resolution, the study of ancient biomolecules has made it possible for us to disentangle the complex processes that shaped the ancient faunal diversity across millennia, with the potential to aid in implicating probable causes of species extinction and how humans impacted the genetics and ecology of wild and domestic species. However, even now, few studies explore interdisciplinary biomolecular approaches to reveal ancient faunal diversity dynamics in relation to environmental and anthropogenic impact. This review will approach how biomolecules have been implemented in a broad variety of topics and species, from the extinct Pleistocene megafauna to ancient wild and domestic stocks, as well as how their future use has the potential to offer an enhanced understanding of drivers of past faunal diversity on Earth.
Ancient DNA studies suggest that Late Pleistocene climatic changes had a significant effect on population dynamics in Arctic species. The Eurasian collared lemming (Dicrostonyx torquatus) is a ...keystone species in the Arctic ecosystem. Earlier studies have indicated that past climatic fluctuations were important drivers of past population dynamics in this species.
Here, we analysed 59 ancient and 54 modern mitogenomes from across Eurasia, along with one modern nuclear genome. Our results suggest population growth and genetic diversification during the early Late Pleistocene, implying that collared lemmings may have experienced a genetic bottleneck during the warm Eemian interglacial. Furthermore, we find multiple temporally structured mitogenome clades during the Late Pleistocene, consistent with earlier results suggesting a dynamic late glacial population history. Finally, we identify a population in northeastern Siberia that maintained genetic diversity and a constant population size at the end of the Pleistocene, suggesting suitable conditions for collared lemmings in this region during the increasing temperatures associated with the onset of the Holocene.
This study highlights an influence of past warming, in particular the Eemian interglacial, on the evolutionary history of the collared lemming, along with spatiotemporal population structuring throughout the Late Pleistocene.
Ancient DNA has significantly improved our understanding of the evolution and population history of extinct megafauna. However, few studies have used complete ancient genomes to examine species ...responses to climate change prior to extinction. The woolly rhinoceros (Coelodonta antiquitatis) was a cold-adapted megaherbivore widely distributed across northern Eurasia during the Late Pleistocene and became extinct approximately 14 thousand years before present (ka BP). While humans and climate change have been proposed as potential causes of extinction 1–3, knowledge is limited on how the woolly rhinoceros was impacted by human arrival and climatic fluctuations 2. Here, we use one complete nuclear genome and 14 mitogenomes to investigate the demographic history of woolly rhinoceros leading up to its extinction. Unlike other northern megafauna, the effective population size of woolly rhinoceros likely increased at 29.7 ka BP and subsequently remained stable until close to the species’ extinction. Analysis of the nuclear genome from a ∼18.5-ka-old specimen did not indicate any increased inbreeding or reduced genetic diversity, suggesting that the population size remained steady for more than 13 ka following the arrival of humans 4. The population contraction leading to extinction of the woolly rhinoceros may have thus been sudden and mostly driven by rapid warming in the Bølling-Allerød interstadial. Furthermore, we identify woolly rhinoceros-specific adaptations to arctic climate, similar to those of the woolly mammoth. This study highlights how species respond differently to climatic fluctuations and further illustrates the potential of palaeogenomics to study the evolutionary history of extinct species.
•Complete genome and mitogenome analysis of the extinct woolly rhinoceros•Demographic analysis suggests stable population size until close to extinction•No increased inbreeding or reduced genomic diversity coinciding with human arrival•Woolly rhinoceros had genetic adaptations to arctic climate
Here, Lord et al. sequence a complete nuclear genome and 14 mitogenomes from the extinct woolly rhinoceros. Demographic analyses show that the woolly rhinoceros population size was large until close to extinction and not affected by modern human arrival in northeastern Siberia. The extinction may have been mostly driven by climate warming.
Ancient DNA (aDNA) has played a major role in our understanding of the past. Important advances in the sequencing and analysis of aDNA from a range of organisms have enabled a detailed understanding ...of processes such as past demography, introgression, domestication, adaptation and speciation. However, to date and with the notable exception of microbiomes and sediments, most aDNA studies have focused on single taxa or taxonomic groups, making the study of changes at the community level challenging. This is rather surprising because current sequencing and analytical approaches allow us to obtain and analyse aDNA from multiple source materials. When combined, these data can enable the simultaneous study of multiple taxa through space and time, and could thus provide a more comprehensive understanding of ecosystem-wide changes. It is therefore timely to develop an integrative approach to aDNA studies by combining data from multiple taxa and substrates. In this review, we discuss the various applications, associated challenges and future prospects of such an approach.
Genomic studies of species threatened by extinction are providing crucial information about evolutionary mechanisms and genetic consequences of population declines and bottlenecks. However, to ...understand how species avoid the extinction vortex, insights can be drawn by studying species that thrive despite past declines. Here, we studied the population genomics of the muskox (Ovibos moschatus), an Ice Age relict that was at the brink of extinction for thousands of years at the end of the Pleistocene yet appears to be thriving today. We analysed 108 whole genomes, including present‐day individuals representing the current native range of both muskox subspecies, the white‐faced and the barren‐ground muskox (O. moschatus wardi and O. moschatus moschatus) and a ~21,000‐year‐old ancient individual from Siberia. We found that the muskox' demographic history was profoundly shaped by past climate changes and post‐glacial re‐colonizations. In particular, the white‐faced muskox has the lowest genome‐wide heterozygosity recorded in an ungulate. Yet, there is no evidence of inbreeding depression in native muskox populations. We hypothesize that this can be explained by the effect of long‐term gradual population declines that allowed for purging of strongly deleterious mutations. This study provides insights into how species with a history of population bottlenecks, small population sizes and low genetic diversity survive against all odds.
The domestic guinea pig (Cavia porcellus) was translocated from South America to several Caribbean islands sometime after 500 CE. Identifying the timing and routes of guinea pig translocation can ...provide a proxy for human interaction in the region. A recent investigation of aDNA of Caribbean guinea pig remains, based on sequences from short regions of the mitochondrial D-loop and cytochrome B regions, suggested a Colombian origin and single introduction of guinea pigs to the Caribbean. Here, we present the first complete mitogenome sequences for three ancient guinea pigs from Puerto Rico, Antigua and Carriacou, as well as for a modern Puerto Rican specimen, which allow us to clarify and expand upon the results of the earlier study. Complete mitogenome sequences indicate that there are at least two different mitochondrial DNA haplotypes in the ancient Caribbean guinea pigs, suggesting two distinct ancient introductions and a modern reintroduction of guinea pigs to Puerto Rico. Our results demonstrate the value of Next Generation Sequencing and the analysis of complete mitogenome sequences to investigate genetic variation and translocation of guinea pigs into the Caribbean.
•Exploring the use of ancient guinea pigs as a commensal model for human interaction•Demonstrates the value of Next Generation Sequencing and complete mitogenomes•Two possible translocations of ancient guinea pigs to the Caribbean
Tokelau is a remote archipelago of atolls in western Polynesia, located approximately 500 km north of Samoa. It is thought to have been settled as part of the Austronesian expansion(s). However, its ...exact role in this population dispersal is not completely understood. Here we describe the results of complete mitochondrial genome sequencing for both the current inhabitants and ancient individuals from the archipelago in addition to an assessment of Y-chromosome diversity among the present population. We find relatively little genetic diversity compared with other western Polynesian populations, most likely due to historically reported bottleneck events. However, the presence of rare mitochondrial lineages hints at prehistoric occupation by peoples from the northwest (e.g., Tuvalu and Micronesia). Ancient DNA data from Atafu, the northernmost Tokelauan atoll, is further consistent with abandonment and later resettlement of the island from a Samoan or Samoan-derived source population. Moreover, the ancient and modern mitogenomes also suggest links with other atoll populations in the western Pacific.
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