Global phylogeography of the insect pest Callosobruchus maculatus (Coleoptera: Bruchinae) relates to the history of its main host, Vigna unguiculata

Aim: The seed beetle Callosobruchus maculatus is an important tropical and subtropical pest of legumes distributed world-wide. Archaeological evidence suggests an African origin with later world-wide invasion facilitated by the last centuries' legume trading and exchange. To date, no studies could identify the routes or timing of dispersal of the species. Here, we investigate the global phylogeography of this pest to shed light on the main inter-continental dispersal routes that led to it becoming a cosmopolitan pest. Location: World-wide. Methods: We sampled seed beetles over a large fraction of the species' range and sequenced one nuclear and three mitochondrial loci. Using this data, we estimated spatio-temporal phylogeographical reconstructions, and the demographic history of the species. We also used our dataset to evaluate the effect of panmixia on Bayesian demographic estimations. Results: Callosobruchus maculatus exhibited regional and continental genetic structure, with the highest genetic diversity found in Africa. Our discrete Bayesian phylogeographical approach indicated that the species first dispersed to Asia and then colonized the pantropical belt. The three methods used for inferring the demographic history of C. maculatus indicated a recent demographic expansion in the world-wide dataset, as well as in the subset restricted to African samples. Such a signal was, however, not observed in the subset composed of Asian specimens. This demographic expansion occurred in the Holocene and is likely explained by the spread of cowpea and other host legumes across and out of Africa. Main conclusions: The inferred dispersal routes support the idea that the evolutionary history of C. maculatus relates to the trade of its main host plant, Vigna unguiculata. Human-mediated processes appear to have shaped the global genetic structure of this pest. As a methodological implication, we demonstrate that coalescent-based demographic reconstructions can be erroneous if the dataset violates the assumption of panmixia.