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

Host-Plant Usage and Anthropogenic Factors. PLoS ONE 9(9): e106268. doi:10.1371/journal.pone.0106268 Global Genetic Differentiation in a Cosmopolitan Pest of Stored Beans: Effects of Geography, Host-Plant Usage and Anthropogenic Factors Midori Tuda 0 Kumiko Kagoshima 0 Yukihiko Toquenaga 0 Go ran Arnqvist 0 Nadir Alvarez, University of Lausanne, Switzerland 0 1 Laboratory of Insect Natural Enemies, Division of Agricultural Bioresource Sciences, Department of Bioresource Sciences, Faculty of Agriculture, Kyushu University , Fukuoka , Japan , 2 Institute of Biological Control, Faculty of Agriculture, Kyushu University , Fukuoka , Japan , 3 Faculty of Agriculture, Kyushu University , Fukuoka , Japan , 4 Faculty of Life and Environmental Sciences, University of Tsukuba , Tsukuba, Ibaraki, Japan, 5 Animal Ecology , Department of Ecology and Evolution, Evolutionary Biology Centre, University of Uppsala , Uppsala , Sweden 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. - Funding: This study was supported by Grants-in-Aid from JSPS (http://www.jsps.go.jp/english/index.html) (17405005, 20405006, 19510237, 22570215, 25430194 and 23405008) to MT and YT and by grants from the Swedish Research Council (http://www.vr.se/inenglish.4.12fff4451215cbd83e4800015152.html) (621-20105266) and the European Research Council (http://erc.europa.eu/) (AdG-294333) to GA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Genetic differentiation can be induced allopatrically by geographic isolation of populations and/or sympatrically by, for example, host-race formation. In crop pests, the trade of crops across the world tends to generate a global mixing of genetic variants in pest populations, whether these were generated and maintained either allopatrically (e.g., [1],[2]) or sympatrically (e.g., [3],[4]). However, the relative contributions of allopatric or sympatric genetic differentiation versus global genotypic intermixing by natural [5] or human-aided [6][8] dispersal to global (continental and island) population structures has rarely been evaluated quantitatively (but see [9],[10]). Association with specific host plants may allow the formation of genetically distinct pest host races in some cases [6], but not in others [5]. It has been suggested that an increased use of dry crops may have led to the multivoltine life cycles, polyphagy and expanded geographic distribution of stored bean pests [11][16]. Among the stored bean pests are several seed beetle species of the genus Callosobruchus (Coleoptera: Chrysomelidae: Bruchinae). Bruchine adults of such species lay eggs on dry seeds of legume crops and larvae burrow into them. Low levels of infestation are difficult to detect because these beetles live inside the seeds as larvae, pupae and pre-emergence adults. Because of the cryptic feeding in grains, world trade of dry beans for human consumption can potentially lead to the effective spread of these beetles. In general, flight distance is correlated with body size in animals [17]. Among insects, beetles are generally weak flyers. For small beetles like seed beetles, the flight distance is limited [18] and longdistance transoceanic dispersal, even via air currents, is considered virtually impossible [19][21]. The low water content of stored beans is known to increase the frequency of the flightless Democratic Republic of the Congo (Zaire)b Host species (nc) Host species (nc) Locations are categorized by regions (continents or archipelagos) and by subregions. a[101]. bexcluded from dataset for AMOVA, IBD test and sudden demographic growth test because of .10 years of laboratory rearing and/or small sample sizes. cnumber of individuals used. doi:10.1371/journal.pone.0106268.t001 (sedentary) form in Callosobruchus populations [22],[23], thus further limiting the dispersal of populations of these beetles. Callosobruchus maculatus (F.) is a major stored bean pest in subSaharan Africa [24],[25]. It is a model organism for studies of behavior, polymorphism, population ecology, and evolutionary biology (e.g., [26][44]). It is considered to be of Afrotropical origin [45]. Its main, and probably ancestral, host is the cowpea Vigna unguiculata (L.) Walp., but other species of Vigna and other cultivated legumes are also infested by the beetle [16],[45]. Recent molecular work has revealed that C. maculatus populations are partially intermixed across agro-ecological zones of Western Africa [46]. The cowpea is a drought-tolerant food crop for humans and livestock feed that is grown throughout the semi-arid tropics [47] [49]. It originated in southeast Africa and expanded its distribution westward and southward [50],[51]. Its domestication is estimated to have taken place in Western Africa based on maximum diversity of cultivated cowpeas [50][52]. It has been estimated that it was brought (...truncated)