Abstract
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.
Highlights
Genetic differentiation can be induced allopatrically by geographic isolation of populations and/or sympatrically by, for example, host-race formation
Study animals Callosobruchus maculatus were collected as adults that emerged from randomly selected cultivated beans collected from local markets in various parts of Africa, the Middle East, South and Southeast Asia, Oceania and South America (Table 1)
There was no sequence variation across C. maculatus individuals in the two fragments of 28S and these were discarded from subsequent analyses
Summary
Genetic differentiation can be induced allopatrically by geographic isolation of populations and/or sympatrically by, for example, host-race formation. 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]). 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. 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
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