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Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors

Genetic differentiation can be promoted allopatrically by geographic isolation of populations due to limited dispersal ability and diversification over time or sympatrically through, for example, host-race formation. In crop pests, the trading of crops across the world can lead to intermixing of gen...

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Autores principales: Tuda, Midori, Kagoshima, Kumiko, Toquenaga, Yukihiko, Arnqvist, Göran
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4152179/
https://www.ncbi.nlm.nih.gov/pubmed/25180499
http://dx.doi.org/10.1371/journal.pone.0106268
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author Tuda, Midori
Kagoshima, Kumiko
Toquenaga, Yukihiko
Arnqvist, Göran
author_facet Tuda, Midori
Kagoshima, Kumiko
Toquenaga, Yukihiko
Arnqvist, Göran
author_sort Tuda, Midori
collection PubMed
description Genetic differentiation can be promoted allopatrically by geographic isolation of populations due to limited dispersal ability and diversification over time or sympatrically through, for example, host-race formation. In crop pests, the trading of crops across the world can lead to intermixing of genetically distinct pest populations. However, our understanding of the importance of allopatric and sympatric genetic differentiation in the face of anthropogenic genetic intermixing is limited. Here, we examined global sequence variation in two mitochondrial and one nuclear genes in the seed beetle Callosobruchus maculatus that uses different legumes as hosts. We analyzed 180 samples from 42 populations of this stored bean pest from tropical and subtropical continents and archipelagos: Africa, the Middle East, South and Southeast Asia, Oceania and South America. For the mitochondrial genes, there was weak but significant genetic differentiation across continents/archipelagos. Further, we found pronounced differentiation among subregions within continents/archipelagos both globally and within Africa but not within Asia. We suggest that multiple introductions into Asia and subsequent intermixing within Asia have generated this pattern. The isolation by distance hypothesis was supported globally (with or without continents controlled) but not when host species was restricted to cowpeas Vigna unguiculata, the ancestral host of C. maculatus. We also document significant among-host differentiation both globally and within Asia, but not within Africa. We failed to reject a scenario of a constant population size in the recent past combined with selective neutrality for the mitochondrial genes. We conclude that mitochondrial DNA differentiation is primarily due to geographic isolation within Africa and to multiple invasions by different alleles, followed by host shifts, within Asia. The weak inter-continental differentiation is most likely due to frequent inter-continental gene flow mediated by human crop trade.
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spelling pubmed-41521792014-09-05 Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors Tuda, Midori Kagoshima, Kumiko Toquenaga, Yukihiko Arnqvist, Göran PLoS One Research Article Genetic differentiation can be promoted allopatrically by geographic isolation of populations due to limited dispersal ability and diversification over time or sympatrically through, for example, host-race formation. In crop pests, the trading of crops across the world can lead to intermixing of genetically distinct pest populations. However, our understanding of the importance of allopatric and sympatric genetic differentiation in the face of anthropogenic genetic intermixing is limited. Here, we examined global sequence variation in two mitochondrial and one nuclear genes in the seed beetle Callosobruchus maculatus that uses different legumes as hosts. We analyzed 180 samples from 42 populations of this stored bean pest from tropical and subtropical continents and archipelagos: Africa, the Middle East, South and Southeast Asia, Oceania and South America. For the mitochondrial genes, there was weak but significant genetic differentiation across continents/archipelagos. Further, we found pronounced differentiation among subregions within continents/archipelagos both globally and within Africa but not within Asia. We suggest that multiple introductions into Asia and subsequent intermixing within Asia have generated this pattern. The isolation by distance hypothesis was supported globally (with or without continents controlled) but not when host species was restricted to cowpeas Vigna unguiculata, the ancestral host of C. maculatus. We also document significant among-host differentiation both globally and within Asia, but not within Africa. We failed to reject a scenario of a constant population size in the recent past combined with selective neutrality for the mitochondrial genes. We conclude that mitochondrial DNA differentiation is primarily due to geographic isolation within Africa and to multiple invasions by different alleles, followed by host shifts, within Asia. The weak inter-continental differentiation is most likely due to frequent inter-continental gene flow mediated by human crop trade. Public Library of Science 2014-09-02 /pmc/articles/PMC4152179/ /pubmed/25180499 http://dx.doi.org/10.1371/journal.pone.0106268 Text en © 2014 Tuda et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Tuda, Midori
Kagoshima, Kumiko
Toquenaga, Yukihiko
Arnqvist, Göran
Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors
title Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors
title_full Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors
title_fullStr Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors
title_full_unstemmed Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors
title_short Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors
title_sort global genetic differentiation in a cosmopolitan pest of stored beans: effects of geography, host-plant usage and anthropogenic factors
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4152179/
https://www.ncbi.nlm.nih.gov/pubmed/25180499
http://dx.doi.org/10.1371/journal.pone.0106268
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