A continuum of genetic divergence from sympatric host races to species in the pea aphid complex

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Abstract
Sympatric populations of insects adapted to different host plants, i.e., host races, are good models to investigate how natural selection can promote speciation in the face of ongoing gene flow. However, host races are documented in very few model systems and their gradual evolution into good species, as assumed under a Darwinian view of species formation, lacks strong empirical support. We aim at resolving this uncertainty by investigating host specialization and gene flow among populations of the pea aphid complex, Acyrthosiphon pisum. Genetic markers and tests of host plant specificity indicate the existence of at least 11 well-distinguished sympatric populations associated with different host plants in Western Europe. Population assignment tests show variable migration and hybridization rates among sympatric populations, delineating 8 host races and 3 possible species. Notably, hybridization correlates negatively with genetic differentiation, forming a continuum of population divergence toward virtually complete speciation. The pea aphid complex thus illustrates how ecological divergence can be sustained among many hybridizing populations and how insect host races blend into species by gradual reduction of gene flow.