Specialized feeding behavior influences both ecological specialization andassortative mating in sympatric host races of pea aphids

Not only is ecological specialization a defining feature of much of Earth's biological diversity, the evolution of specialization may also play a cent ral role in generating diversity by facilitating speciation. To understand how ecological specialization evolves, we must know the particular characte rs that cause organisms to be specialized. For example, most theories of sp ecialization in herbivorous insects emphasize physiological trade-offs in r esponse to toxic plant chemicals. However, even in herbivores, it is likely that other characters are also involved in resource specialization. Knowin g the causes of ecological specialization is also crucial for linking speci alization to speciation. When the same character(s) that cause specializati on also influence assortative mating, speciation may occur particularly rap idly because specialization and reproductive isolation become coupled in a positive feedback that speeds the evolution of both. Indeed, a central hypo thesis in the study of ecological speciation is that specialization in rece ntly diverged taxa may often be due to characters that also produce assorta tive mating. We test this hypothesis by evaluating the causes of ecological specialization among host-associated populations of an herbivorous insect, the pea aphid (Acyrthosiphon pisum). These populations are highly speciali zed on different host plants (alfalfa or clover; "alternate hosts"), and th e races are partially reproductively isolated. Here, we identify key charac ters responsible for host plant specialization. Our results suggest that th e major proximal determinant of host specialization is the behavioral accep tance of a plant rather than the toxicity of the food source. Pea aphids ra pidly assess alfalfa and clover and reject the alternate host based on chem ical cues that are perceived before the initiation of feeding. This rapid b ehavioral rejection of the alternate host by a given race has two consequen ces. First, unrestrained aphids quickly leave the alternate host and search for other plants. Because pea aphids mate on their host plants, divergence in host acceptance among ecologically specialized races leads to congregat ion on the favored host. This results in de facto assortative mating when s exual forms are produced in late summer. Second, specialized aphids that ar e held on the alternate host will not leed in a 7.2-h trial, even in the fa ce of starvation. Thus, a complex trait, behavioral acceptance of a plant a s host, influences both reproductive isolation (through host-associated ass ortative mating) and ecological specialization (because of low nutritional uptake on the alternate host). This dual influence of feeding behavior on b oth assortative mating and resource specialization is central to the mainte nance of these divergent races, and it may also have been involved in their origin.