An emerging example of tritrophic coevolution between flies (Diptera: Fergusoninidae) and nematodes (Nematoda: Neotylenchidae) on Myrtaceae host plants

Abstract

A unique obligate mutualism occurs between species of Fergusonina Malloch flies (Diptera: Fergusoninidae) and nematodes of the genus Fergusobia Currie (Nematoda: Neotylenchidae). These mutualists together form different types of galls on Myrtaceae, mainly in Australia. The galling association is species-specific, and each mutualism in turn displays host specificity. This tritrophic system represents a compelling arena to test hypotheses about coevolution between the host plants, parasitic nematodes and the fergusoninid flies, and the evolution of these intimate mutualisms. We have a basic knowledge of the interactions between the host plant, fly and nematode in this system, but a more sophisticated understanding will require a much more intensive and coordinated research effort. Summaries of the known Fergusonina/Fergusobia species associations and gall type terminology are presented. This paper identifies the key advantages of the system and questions to be addressed, and proposes a number of predictions about the evolutionary dynamics of the system given our understanding of the biology of the mutualists. Future research will profitably focus on (1) gall cecidogenesis and phenology, (2) the interaction between the fly larva and the nematode in the gall, and between the adult female fly and the parasitic nematode, (3) the means by which the fly and nematode life cycles are coordinated, (4) a targeted search of groups in the plant family Myrtaceae that have not yet been identified as gall hosts, and (5) establishment and comparison of the phylogenetic relationships of the host plants, fly species and nematodes. Recently derived phylogenies and divergence time estimation studies of the Diptera and the Myrtaceae show that the fly family Fergusoninidae is less than half the age of the Myrtaceae, discounting the hypothesis of cospeciation and coradiation of the fly/nematode mutualism and the plants at the broadest levels. However, cospeciation may have occurred at shallower levels in the phylogeny, following the establishment of the fly/nematode mutualism on the Myrtaceae.