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. 2022 Jun 23;18(6):e1010243.
doi: 10.1371/journal.pgen.1010243. eCollection 2022 Jun.

Reconstructing the history of founder events using genome-wide patterns of allele sharing across individuals

Rémi Tournebize  1   2 , Gillian Chu  3 , Priya Moorjani  1   2
Affiliations

Reconstructing the history of founder events using genome-wide patterns of allele sharing across individuals

Rémi Tournebize et al. PLoS Genet. .

Abstract

Founder events play a critical role in shaping genetic diversity, fitness and disease risk in a population. Yet our understanding of the prevalence and distribution of founder events in humans and other species remains incomplete, as most existing methods require large sample sizes or phased genomes. Thus, we developed ASCEND that measures the correlation in allele sharing between pairs of individuals across the genome to infer the age and strength of founder events. We show that ASCEND can reliably estimate the parameters of founder events under a range of demographic scenarios. We then apply ASCEND to two species with contrasting evolutionary histories: ~460 worldwide human populations and ~40 modern dog breeds. In humans, we find that over half of the analyzed populations have evidence for recent founder events, associated with geographic isolation, modes of sustenance, or cultural practices such as endogamy. Notably, island populations have lower population sizes than continental groups and most hunter-gatherer, nomadic and indigenous groups have evidence of recent founder events. Many present-day groups--including Native Americans, Oceanians and South Asians--have experienced more extreme founder events than Ashkenazi Jews who have high rates of recessive diseases due their known history of founder events. Using ancient genomes, we show that the strength of founder events differs markedly across geographic regions and time--with three major founder events related to the peopling of Americas and a trend in decreasing strength of founder events in Europe following the Neolithic transition and steppe migrations. In dogs, we estimate extreme founder events in most breeds that occurred in the last 25 generations, concordant with the establishment of many dog breeds during the Victorian times. Our analysis highlights a widespread history of founder events in humans and dogs and elucidates some of the demographic and cultural practices related to these events.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. ASCEND simulation results.
(A) Model of founder event. Consider a population which has experienced a founder event in its past. This history can be divided into three main periods (from the most ancient to the most recent): a period Po where the population has a constant effective population size of No, followed by a period Pb where the effective population size reduces to Nf for the duration of Df generations till Tf generations before present. Then, the population recovers and the population size returns to No during the period PP. We simulated two populations, population A (target) which experienced a founder event and population O (outgroup, no founder event, with constant size No) that diverged 1,800 generations ago. We ran ASCEND and compared the estimated parameters with the true parameters of the founder event in population A. (B) Accuracy in estimating founder age. The X-axis shows the true founder age that was simulated in generations before present (gBP) and the Y-axis shows the founder age estimated by ASCEND. The diagonal represents the expectation (i.e., the case where the estimated values are the same as the true values). We note that for Df > 0 we show a thick band for the diagonal, proportional to duration of the founder event. (C) Accuracy in estimating founder intensity. We define the founder intensity as the ratio of the bottleneck duration over twice the effective population size during the bottleneck, i.e. If = Df/(2Nf). The X-axis shows the true founder intensity, and the Y-axis shows the estimated founder intensity. The diagonal represents the expectation (i.e., the case where the estimated values are the same as the true values).
Fig 2
Fig 2. History of founder events in present-day human populations.
Results of ASCEND for present-day populations in the Human Origins v37 dataset that passed filtering criteria and showed significant evidence of founder events (see Methods). Each point shown represents a population and the vertical segment represents the age of its associated founder event (where the segment length is proportional to the founder age). To avoid overplotting in certain areas, we shifted the location of a few populations and indicated their original location (black diamond point) with an arrow getting darker towards the original location. The color gradient of the points and segments is proportional to the estimated founder intensity. Points with a black border represent populations which have experienced significantly stronger founder events than Ashkenazi Jews (shown in legend for reference). The strongest founder event is estimated for the Andamanese population Onge (21.2%). The world map was obtained from the R package maps with GPL-2 public license.
Fig 3
Fig 3. Geographic and cultural practices impact founder events in humans.
We show the variation in estimated founder intensity as a violin plot across groups, classified in three plots. Each violin plot includes a boxplot and the number of populations (n) in each group along with the mean ± standard deviation and the total number of individuals used in the analysis. Note that within each panel, the areas of violins are the same. (A) Continental vs. island populations. This plot shows the variation in founder intensities estimated for present-day populations in the HO37 dataset classified according to geography. (B) Tribal vs. non-tribal groups in South Asia. This plot shows the variation in founder intensities estimated in the South Asian groups from the IndiaHO dataset. (C) Ancient hunter-gatherers, Near Easter farmers, European Neolithic farmers, Steppe pastoralists and Bronze Age populations. This plot shows the variation in estimated founder intensities for ancient groups in the HO44 dataset, classified based on their mode of sustenance. Below the number of individuals used in the analysis, we report the median radiocarbon age of each category in years BP (yBP). We note that in order to increase the number of groups in each category, we considered populations where the estimated founder age was dated below 300 generations before sampling age (default for other analyses was below 200 generations).
Fig 4
Fig 4. History of extreme founder events in dogs.
Results of ASCEND for all dog breeds that passed the filtering criteria and showed evidence for significant founder events in the Hayward dataset (see Methods). The breeds are grouped according to their role as reported by the American Kennel Club database. The outer (colored) rim represents the founder intensity, with bar height proportional to the founder intensity. Note that within each role category, breeds are classified by decreasing founder intensity in the clockwise direction. The inner (gray) rim represents the founder age (in generations before present), with the bar height proportional to the founder age. The width of the bars is inversely proportional to the number of breeds within each role category. Icons were retrieved from openclipart.org.
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