Evolution of oviposition strategies and speciation in the globeflower flies Chiastocheta spp. (Anthomyiidae)

Trollius europaeus (Ranunculaceae) is involved in an intimate interaction with several species of Chiastocheta flies (Anthomyiidae) that are both seed predators and pollinators. In this paper, we analyse the oviposition strategy of the six Chiastocheta species found to coexist on T. europaeus in 19 populations from the French Alps. We show that the species are not equivalent in their oviposition behaviour: C. rotundiventris usually deposits no more than one egg per flower in first-day flowers whereas C. dentifera aggregates its eggs on fruits and thus does not contribute to pollination at all; the four remaining species deposit eggs sequentially during the flowering period from the 2nd to the 7th day. Hence, the outcomes of the interaction in terms of net seed production for the plant greatly depend on the Chiastocheta species visiting it, ranging from a mutualistic to a purely parasitic interaction. We assessed mitochondrial divergence between Chiastocheta spp. by sequencing a 1320-bp mitochondrial DNA fragment. The low divergence observed between species (0–4.15%) suggests that genus diversification took place recently. Unlike in other plant–insect systems where diversification is usually thought to be driven by cospeciation or host shifts, we propose that Chiastocheta speciation took place within the host plant. Basal separation of a particularly mutualistic species provided favourable conditions for plant specialization on this seed-parasite as a pollinator early in the evolution of the association. The parasitic species ovipositing on fruits derived from a species ovipositing on flowers. Diversification of the intermediate strategies probably occurred in relation with the Pleistocene climatic events, reproductive isolation between species being reinforced by niche partitioning for oviposition and/or sexual selection.