Host races of the pea aphid Acyrthosiphon pisum differ in male wing phenotypes

The evolution of reproductive isolation without geographic isolation (sympatric speciation) has recently gained strong theoretical and empirical supports. It is now widely admitted that many host-specific phytophagous insect species have arisen through shifting and adapting to new plants. The pea aphid Acyrthosiphon pisum has received considerable attention in this context and is now considered as a probable case of incipient sympatric speciation through host specialization. In Europe, three host races have been described so far, one on annual plants (pea and broad bean) and two on perennial plants (red clover and alfalfa, respectively). These host races are genetically differentiated and exhibit strong ecological specialization affecting their preferences and performances on alternative plants. Here, we investigate whether other life-history traits of ecological importance are associated with host specialization in the species. In particular, because A. pisum shows a genetically determined male wing variation, we tested if its host races also differ in their proportion of winged/wingless male phenotypes. We used a large collection of pea aphid lineages sampled on pea, broad bean, red clover and alfalfa and analyzed their male production by placing them in conditions inducing the sexual phase in A. pisum. Striking differences in the frequency of male dispersal genotypes were found between host populations; aphids producing winged males were in high proportion among lineages from annual hosts, while those producing wingless males were in high proportion on perennial ones. The evolutionary maintenance and ecological consequences of this association between habitat specialization and male wing variation are discussed.