The spatiotemporal patterns of major human admixture events during the European Holocene

  1. Manjusha Chintalapati  Is a corresponding author
  2. Nick Patterson  Is a corresponding author
  3. Priya Moorjani  Is a corresponding author
  1. University of California, Berkeley, United States
  2. Broad Institute, United States

Abstract

Recent studies have shown that admixture has been pervasive throughout human history. While several methods exist for dating admixture in contemporary populations, they are not suitable for sparse, low coverage ancient genomic data. Thus, we developed DATES that leverages ancestry covariance patterns across the genome of a single individual to infer the timing of admixture. DATES provides reliable estimates under various demographic scenarios and outperforms available methods for ancient DNA applications. Using DATES on ~1,100 ancient genomes, we reconstruct major gene flow events during European Holocene. By studying the genetic formation of Anatolian farmers, we infer that gene flow related to Iranian Neolithic farmers occurred before 9,600 BCE, predating the advent of agriculture in Anatolia. Contrary to the archaeological evidence, we estimate that early Steppe pastoralist groups (Yamnaya and Afanasievo) were genetically formed more than a millennium before the start of steppe pastoralism. Using time transect samples across sixteen regions, we provide a fine-scale chronology of the Neolithization of Europe and the rapid spread of Steppe pastoralist ancestry across Europe. Our analyses provide new insights on the origins and spread of farming and Indo-European languages, highlighting the power of genomic dating methods to elucidate the legacy of human migrations.

Data availability

All data analyzed during this study is publicly available at: https://reich.hms.harvard.edu/allen-ancient-dna-resource-aadr-downloadable-genotypes-present-day-and-ancient-dna-data

Article and author information

Author details

  1. Manjusha Chintalapati

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    m_chintalapati@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Nick Patterson

    Program in Medical and Population Genetics, Broad Institute, Cambridge, United States
    For correspondence
    nickp@broadinstitute.org
    Competing interests
    The authors declare that no competing interests exist.
  3. Priya Moorjani

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    moorjani@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0947-5673

Funding

National Institutes of Health (R35GM142978)

  • Priya Moorjani

Burroughs Wellcome Fund (Career Award at the Scientific Interface)

  • Priya Moorjani

Alfred P. Sloan Foundation (Sloan Research Fellowship)

  • Priya Moorjani

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Version history

  1. Preprint posted: January 20, 2022 (view preprint)
  2. Received: February 5, 2022
  3. Accepted: May 29, 2022
  4. Accepted Manuscript published: May 30, 2022 (version 1)
  5. Version of Record published: July 18, 2022 (version 2)

Copyright

© 2022, Chintalapati et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,561
    views
  • 1,218
    downloads
  • 28
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Manjusha Chintalapati
  2. Nick Patterson
  3. Priya Moorjani
(2022)
The spatiotemporal patterns of major human admixture events during the European Holocene
eLife 11:e77625.
https://doi.org/10.7554/eLife.77625

Share this article

https://doi.org/10.7554/eLife.77625

Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics
    Brian PH Metzger, Yeonwoo Park ... Joseph W Thornton
    Research Article

    A protein’s genetic architecture – the set of causal rules by which its sequence produces its functions – also determines its possible evolutionary trajectories. Prior research has proposed that the genetic architecture of proteins is very complex, with pervasive epistatic interactions that constrain evolution and make function difficult to predict from sequence. Most of this work has analyzed only the direct paths between two proteins of interest – excluding the vast majority of possible genotypes and evolutionary trajectories – and has considered only a single protein function, leaving unaddressed the genetic architecture of functional specificity and its impact on the evolution of new functions. Here, we develop a new method based on ordinal logistic regression to directly characterize the global genetic determinants of multiple protein functions from 20-state combinatorial deep mutational scanning (DMS) experiments. We use it to dissect the genetic architecture and evolution of a transcription factor’s specificity for DNA, using data from a combinatorial DMS of an ancient steroid hormone receptor’s capacity to activate transcription from two biologically relevant DNA elements. We show that the genetic architecture of DNA recognition consists of a dense set of main and pairwise effects that involve virtually every possible amino acid state in the protein-DNA interface, but higher-order epistasis plays only a tiny role. Pairwise interactions enlarge the set of functional sequences and are the primary determinants of specificity for different DNA elements. They also massively expand the number of opportunities for single-residue mutations to switch specificity from one DNA target to another. By bringing variants with different functions close together in sequence space, pairwise epistasis therefore facilitates rather than constrains the evolution of new functions.

    1. Evolutionary Biology
    Raphael Aguillon, Mieka Rinsky ... Oren Levy
    Research Article

    The circadian clock enables anticipation of the day/night cycle in animals ranging from cnidarians to mammals. Circadian rhythms are generated through a transcription-translation feedback loop (TTFL or pacemaker) with CLOCK as a conserved positive factor in animals. However, CLOCK’s functional evolutionary origin and mechanism of action in basal animals are unknown. In the cnidarian Nematostella vectensis, pacemaker gene transcript levels, including NvClk (the Clock ortholog), appear arrhythmic under constant darkness, questioning the role of NvCLK. Utilizing CRISPR/Cas9, we generated a NvClk allele mutant (NvClkΔ), revealing circadian behavior loss under constant dark (DD) or light (LL), while maintaining a 24 hr rhythm under light-dark condition (LD). Transcriptomics analysis revealed distinct rhythmic genes in wild-type (WT) polypsunder LD compared to DD conditions. In LD, NvClkΔ/Δ polyps exhibited comparable numbers of rhythmic genes, but were reduced in DD. Furthermore, under LD, the NvClkΔ/Δ polyps showed alterations in temporal pacemaker gene expression, impacting their potential interactions. Additionally, differential expression of non-rhythmic genes associated with cell division and neuronal differentiation was observed. These findings revealed that a light-responsive pathway can partially compensate for circadian clock disruption, and that the Clock gene has evolved in cnidarians to synchronize rhythmic physiology and behavior with the diel rhythm of the earth’s biosphere.