The phylogeny of a mutualism: evolution and coadaptation between Trollius and its seed-parasitic pollinators

Abstract

Interactions between seed-parasitic pollinators and their hosts provide useful model systems for the analysis of evolution of mutualism and potential coevolution between plants and insects. Here I present the systematics, pollination ecology and evolution of one of these interactions. I have documented and analysed the phylogenetic and geographic associations between Trollius (Ranunculaceae: 18 spp.) and Chiastocheta (Diptera: Anthomyiidae; 17 spp.), a host-specific genus of seed-parasitic flies that pollinate their host plants to varying extent. Their interactions are usually facultative mutualisms, but in the specialized T. europaeus three fly species are obligate mutualists and a fourth species is an antagonist. The distribution patterns of fly species among Trollius species suggest that the flies evolved in associations with five highly derived Trollius species, and secondarily colonized four more primitive taxa in the parts of their ranges that overlapped with primary hosts. In general, host specificity is maintained primarily through allopatry, with colonization occurring in regions of overlap between parapatric taxa. Fly speciation has occurred in allopatry, both within and among host taxa. Cospeciation is not evident, but convergent evolution in Trollius flowers of several traits, viz. orange sepals, elongated staminodia and increased carpel number per flower, may be the result of mutualism with Chiastocheta.