A coalescent sampler successfully detects biologically meaningful population structure overlooked by F‐statistics

Abstract Assessing the geographic structure of populations has relied heavily on Sewell Wright's F‐statistics and their numerous analogues for many decades. However, it is well appreciated that, due to their nonlinear relationship with gene flow, F‐statistics frequently fail to reject the null...

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Main Authors: Eric D. Crandall, Robert J. Toonen, ToBo Laboratory, Kimberly A. Selkoe
Format: Article
Language:English
Published: Wiley 2019-02-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.12712
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spelling doaj-ea3bc8e1168e4d39a04fd0af98eff54b2020-11-25T02:59:28ZengWileyEvolutionary Applications1752-45712019-02-0112225526510.1111/eva.12712A coalescent sampler successfully detects biologically meaningful population structure overlooked by F‐statisticsEric D. Crandall0Robert J. Toonen1ToBo Laboratory2Kimberly A. Selkoe3School of Natural Sciences California State University, Monterey Bay Seaside CaliforniaSchool of Ocean and Earth Science and Technology, Hawai‘i Institute of Marine Biology University of Hawai‘i at Manoa Kane‘ohe HawaiiSchool of Ocean and Earth Science and Technology, Hawai‘i Institute of Marine Biology University of Hawai‘i at Manoa Kane‘ohe HawaiiNational Center for Ecological Analysis and Synthesis Santa Barbara CaliforniaAbstract Assessing the geographic structure of populations has relied heavily on Sewell Wright's F‐statistics and their numerous analogues for many decades. However, it is well appreciated that, due to their nonlinear relationship with gene flow, F‐statistics frequently fail to reject the null model of panmixia in species with relatively high levels of gene flow and large population sizes. Coalescent genealogy samplers instead allow a model‐selection approach to the characterization of population structure, thereby providing the opportunity for stronger inference. Here, we validate the use of coalescent samplers in a high gene flow context using simulations of a stepping‐stone model. In an example case study, we then re‐analyze genetic datasets from 41 marine species sampled from throughout the Hawaiian archipelago using coalescent model selection. Due to the archipelago's linear nature, it is expected that most species will conform to some sort of stepping‐stone model (leading to an expected pattern of isolation by distance), but F‐statistics have only supported this inference in ~10% of these datasets. Our simulation analysis shows that a coalescent sampler can make a correct inference of stepping‐stone gene flow in nearly 100% of cases where gene flow is ≤100 migrants per generation (equivalent to FST = 0.002), while F‐statistics had mixed results. Our re‐analysis of empirical datasets found that nearly 70% of datasets with an unambiguous result fit a stepping‐stone model with varying population sizes and rates of gene flow, although 37% of datasets yielded ambiguous results. Together, our results demonstrate that coalescent samplers hold great promise for detecting weak but meaningful population structure, and defining appropriate management units.https://doi.org/10.1111/eva.12712coalescent samplergene flowisolation by distancemtDNApopulation structuresimulation
collection DOAJ
language English
format Article
sources DOAJ
author Eric D. Crandall
Robert J. Toonen
ToBo Laboratory
Kimberly A. Selkoe
spellingShingle Eric D. Crandall
Robert J. Toonen
ToBo Laboratory
Kimberly A. Selkoe
A coalescent sampler successfully detects biologically meaningful population structure overlooked by F‐statistics
Evolutionary Applications
coalescent sampler
gene flow
isolation by distance
mtDNA
population structure
simulation
author_facet Eric D. Crandall
Robert J. Toonen
ToBo Laboratory
Kimberly A. Selkoe
author_sort Eric D. Crandall
title A coalescent sampler successfully detects biologically meaningful population structure overlooked by F‐statistics
title_short A coalescent sampler successfully detects biologically meaningful population structure overlooked by F‐statistics
title_full A coalescent sampler successfully detects biologically meaningful population structure overlooked by F‐statistics
title_fullStr A coalescent sampler successfully detects biologically meaningful population structure overlooked by F‐statistics
title_full_unstemmed A coalescent sampler successfully detects biologically meaningful population structure overlooked by F‐statistics
title_sort coalescent sampler successfully detects biologically meaningful population structure overlooked by f‐statistics
publisher Wiley
series Evolutionary Applications
issn 1752-4571
publishDate 2019-02-01
description Abstract Assessing the geographic structure of populations has relied heavily on Sewell Wright's F‐statistics and their numerous analogues for many decades. However, it is well appreciated that, due to their nonlinear relationship with gene flow, F‐statistics frequently fail to reject the null model of panmixia in species with relatively high levels of gene flow and large population sizes. Coalescent genealogy samplers instead allow a model‐selection approach to the characterization of population structure, thereby providing the opportunity for stronger inference. Here, we validate the use of coalescent samplers in a high gene flow context using simulations of a stepping‐stone model. In an example case study, we then re‐analyze genetic datasets from 41 marine species sampled from throughout the Hawaiian archipelago using coalescent model selection. Due to the archipelago's linear nature, it is expected that most species will conform to some sort of stepping‐stone model (leading to an expected pattern of isolation by distance), but F‐statistics have only supported this inference in ~10% of these datasets. Our simulation analysis shows that a coalescent sampler can make a correct inference of stepping‐stone gene flow in nearly 100% of cases where gene flow is ≤100 migrants per generation (equivalent to FST = 0.002), while F‐statistics had mixed results. Our re‐analysis of empirical datasets found that nearly 70% of datasets with an unambiguous result fit a stepping‐stone model with varying population sizes and rates of gene flow, although 37% of datasets yielded ambiguous results. Together, our results demonstrate that coalescent samplers hold great promise for detecting weak but meaningful population structure, and defining appropriate management units.
topic coalescent sampler
gene flow
isolation by distance
mtDNA
population structure
simulation
url https://doi.org/10.1111/eva.12712
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