The population genomic legacy of the second plague pandemic

Gopalakrishnan, Shyam; Ebenesersdóttir, S. Sunna; Lundstrøm, Inge; Turner‐Walker, Gordon; Moore, Kristjan H. S.; Luisi, Pierre; Martin, Michael D.; Ellegaard, Martin R.; Magnússon, Ólafur Þ.; Sigurðsson, Ásgeir; Snorradóttir, Steinunn; Magnúsdóttir, Droplaug N; Laffoon, Jason E.; Dorp, Lucy van; Liu, Xiaodong; Moltke, Ida; Ávila‐Arcos, María C.; Schraiber, Joshua G.; Rasmussen, Simon; Juan, David; Gelabert, Pere; de-Dios, Toni; Fotakis, Anna K.; Iraeta-Orbegozo, Miren; Vågene‬, Åshild J.; Denham, Sean Dexter; Christophersen, Axel; Stenøien, Hans K.; Vieira, Filipe Garrett; Liu, Shanlin; Günther, Torsten; Kivisild, Toomas; Moseng, Ole Georg; Skår, Birgitte; Cheung, Christina; Sandoval-Velasco, Marcela; Wales, Nathan; Schroeder, Hannes; Campos, Paula F.; Guðmundsdóttir, Valdís B.; Sicheritz-Pontén, Thomas; Petersen, Bent; Halgunset, Jostein; Gilbert, Edmund; Cavalleri, Gianpiero L.; Hovig, Eivind; Kockum, Ingrid; Olsson, Tomas; Alfredsson, Lars; Hansen, Thomas; Werge, Thomas; Willerslev, Eske; Balloux, François; Lalueza‐Fox, Carles; Nielsen, Rasmus; Stefánsson, Kāri; Helgason, Agnar; Gilbert, Martin

doi:10.1016/j.cub.2022.09.023

Cited by 16 publications

(21 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We took several steps to counteract these challenges. First, we confirmed that two common features of ancient DNA datasets: reduced average sequence lengths and low coverage, did not generate reference genome mapping biases (Gopalakrishnan et al 2022) in our historical dataset (Fig. S2).…”

Section: Historical Dna Biasessupporting

confidence: 75%

Genetic load and adaptive potential of a recovered avian species that narrowly avoided extinction

Femerling

Oosterhout

Feng

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

High genetic diversity is often a good predictor of long-term population viability, yet some species persevere despite having low genetic diversity. Here we study the genomic erosion of the Seychelles paradise flycatcher (Terpsiphone corvina), a species that narrowly avoided extinction after having declined to 28 individuals in the 1960s. The species recovered unassisted to over 250 individuals in the 1990s and was downlisted from Critically Endangered to Vulnerable in the IUCN Red List in 2020. By comparing historical, pre-bottleneck (130+ years old) and modern genomes, we uncovered a 10-fold loss of genetic diversity. The genome shows signs of historical inbreeding during the bottleneck in the 1960s, but low levels of recent inbreeding after the demographic recovery. We show that the proportion of severely deleterious mutations has reduced in modern individuals, but mildly deleterious mutations have remained unchanged. Computer simulations suggest that the Seychelles paradise flycatcher avoided extinction and recovered due to its long-term small Ne. This reduced the masked load and made the species more resilient to inbreeding. However, we also show that the chronically small Ne and the severe bottleneck resulted in very low genetic diversity in the modern population. Our simulations show this is likely to reduce the species' adaptive potential when faced with environmental change, thereby compromising its long-term population viability. In light of rapid global rates of population decline, our work highlights the importance of considering genomic erosion and computer modelling in conservation assessments.

show abstract

Section: Historical Dna Biasessupporting

confidence: 75%

Genetic load and adaptive potential of a recovered avian species that narrowly avoided extinction

Femerling

Oosterhout

Feng

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…If there were in reality no difference in allele frequency, the probability of observing an F ST at least as high as the value of 0.0247 observed for rs2549794 with the available pre-vs post-Black Death London sample sizes and perfect genotype information would be approximately P = 0.067 ( Methods, Figure 3A ). This is likely an underestimate since in reality low coverage data, genetic drift and reference bias [9] could lead to inflated F ST values. The large point estimate of the selection coefficient—approximately five times larger than that at the lactase persistence allele [10] which is the largest selection coefficient at a common variant documented in humans to date—is likely simply a consequence of the fact that candidate variants were required to have large estimated F ST values and is not an independent piece of evidence for selection ( Figure 3B ).…”

Section: The Signal Of Enrichment Of Unusual Frequency Changes At Imm...mentioning

confidence: 99%

“…These include a scan based on time series of ancient DNA (rs2549794 empirical P = 0.18) [10], the singleton density score based on high coverage sequence data (rs2549794 Z=1.33, P = 0.09) [18] and a scan based on estimated coalescent times in UK Biobank (minimum P value within 1Mb 0.40) [19]. The locus also failed to replicate in two independent studies of ancient genomes from before and after the Black Death in Britain and Norway [9, 20].…”

Section: The Signal Of Enrichment Of Unusual Frequency Changes At Imm...mentioning

confidence: 99%

Insufficient evidence for natural selection associated with the Black Death

Barton

Santander

Skoglund

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

Klunk et al. analyzed ancient DNA data from individuals in London and Denmark before, during and after the Black Death [1], and argued that allele frequency changes at immune genes were too large to be produced by random genetic drift and thus must reflect natural selection. They also identified four specific variants that they claimed show evidence of selection including at ERAP2, for which they estimate a selection coefficient of 0.39-several times larger than any selection coefficient on a common human variant reported to date. Here we show that these claims are unsupported for four reasons. First, the signal of enrichment of large allele frequency changes in immune genes comparing people in London before and after the Black Death disappears after an appropriate randomization test is carried out: the P value increases by ten orders of magnitude and is no longer significant. Second, a technical error in the estimation of allele frequencies means that none of the four originally reported loci actually pass the filtering thresholds. Third, the filtering thresholds do not adequately correct for multiple testing. Finally, in the case of the ERAP2 variant rs2549794, which Klunk et al. show experimentally may be associated with a host interaction with Y. pestis, we find no evidence of significant frequency change either in the data that Klunk et al. report, or in published data spanning 2,000 years. While it remains plausible that immune genes were subject to natural selection during the Black Death, the magnitude of this selection and which specific genes may have been affected remains unknown.

show abstract

“…The golden eagle was deliberately chosen as the reference to minimize the potential of mapping biases (Gopalakrishnan et al, 2017) and because its assembly is more complete than that of the white-tailed eagle. The available white-tailed eagle genomes originate from Greenland, UK, and Germany, and thus are not equally related to all populations studied here and might introduce errors in the analyses, that is, reference bias (Gopalakrishnan et al, 2017(Gopalakrishnan et al, , 2022. The golden eagle genome has also been assembled to chromosome-level completeness and annotated, thus enabling us both to identify and exclude sex chromosomes in some downstream analyses and to identify the genes present in regions under selection.…”

Section: Materials S and Me Thodsmentioning

confidence: 99%

Genomic diversity and differentiation between island and mainland populations of white‐tailed eagles (Haliaeetus albicilla)

et al. 2023

Self Cite

View full text Add to dashboard Cite

Divergence in the face of high dispersal capabilities is a documented but poorly understood phenomenon. The white‐tailed eagle (Haliaeetus albicilla) has a large geographic dispersal capability and should theoretically be able to maintain genetic homogeneity across its dispersal range. However, following analysis of the genomic variation of white‐tailed eagles, from both historical and contemporary samples, clear signatures of ancient biogeographic substructure across Europe and the North‐East Atlantic is observed. The greatest genomic differentiation was observed between island (Greenland and Iceland) and mainland (Denmark, Norway and Estonia) populations. The two island populations share a common ancestry from a single mainland population, distinct from the other sampled mainland populations, and despite the potential for high connectivity between Iceland and Greenland they are well separated from each other and are characterized by inbreeding and little variation. Temporal differences also highlight a pattern of regional populations persisting despite the potential for admixture. All sampled populations generally showed a decline in effective population size over time, which may have been shaped by four historical events: (1) Isolation of refugia during the last glacial period 110–115,000 years ago, (2) population divergence following the colonization of the deglaciated areas ~10,000 years ago, (3) human population expansion, which led to the settlement in Iceland ~1100 years ago, and (4) human persecution and exposure to toxic pollutants during the last two centuries.

show abstract

The population genomic legacy of the second plague pandemic

Cited by 16 publications

References 48 publications

Genetic load and adaptive potential of a recovered avian species that narrowly avoided extinction

Genetic load and adaptive potential of a recovered avian species that narrowly avoided extinction

Insufficient evidence for natural selection associated with the Black Death

Genomic diversity and differentiation between island and mainland populations of white‐tailed eagles (Haliaeetus albicilla)

Contact Info

Product

Resources

About