Abstract
Among global changes induced by human activities, association of breakdown of geographical barriers and impoverishered biodiversity of agroecosystems may have a strong evolutionary impact on pest species. As a consequence of trade networks' expansion, secondary contacts between incipient species, if hybrid incompatibility is not yet reached, may result in hybrid swarms, even more when empty niches are available as usual in crop fields and farms. By providing important sources of genetic novelty for organisms to adapt in changing environments, hybridization may be strongly involved in the emergence of invasive populations.Because national and international trade networks offered multiple hybridization opportunities during the previous and current centuries, population structure of many pest species is expected to be the most intricate and its inference often blurred when using fast-evolving markers. Here we show that mito-nuclear sequence datasets may be the most helpful in disentangling successive layers of admixture in the composition of pest populations. As a model we used D. gallinae s. l., a mesostigmatid mite complex of two species primarily parasitizing birds, namely D. gallinae L1 and D. gallinae s. str. The latter is a pest species, considered invading layer farms in Brazil. The structure of the pest as represented by isolates from both wild and domestic birds, from European (with a focus on France), Australian and Brazilian farms, revealed past hybridization events and very recent contact between deeply divergent lineages. The role of wild birds in the dissemination of mites appears to be null in European and Australian farms, but not in Brazilian ones. In French farms, some recent secondary contact is obviously consecutive to trade flows. Scenarios of populations' history were established, showing five different combinations of more or less dramatic bottlenecks and founder events, nearly interspecific hybridizations and recent population mixing within D. gallinae s. str.
Highlights
Some global changes induced by human activities impact the evolution of pest species and may have strong incidence on their population genetic structure
Our results have helped conclude that: (1) isolated D. gallinae L1 and several mutually interadmixed lineages have radiated at the same moment, before hybridization, (2) extensive gene flows have recently occurred between distant farms, including at the intercontinental level, (3) gene flows are very reduced, if not null, between wild and domestic birds in Europe, (4) mite populations sampled in Brazilian layer farms seem to result from multiple introduction events, including both wild and domestic origins and (5) mite populations from French farms result from very recent secondary contact between isolated populations, through a NW-SE axis
As opposed to European and Australian patterns, some multiple introduction events from both wild and domestic birds seem to have occurred in Brazil
Summary
Some global changes induced by human activities impact the evolution of pest species and may have strong incidence on their population genetic structure. As a consequence, decreasing diversification in production systems and extension of crop and animal trade networks provide growing numbers of opportunities for long separated pest populations to get in contact within anthropized areas and is susceptible to suddenly and repeatedly generate introgressive hybridization. This may involve deeply diverging lineages if intrinsic zygotic incompatibility was not yet reached
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