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

item NELSON, L. - Commonwealth Scientific And Industrial Research Organisation (CSIRO)
item DAVIES, K. - University Of Adelaide
item Scheffer, Sonja
item TAYLOR, G. - University Of Adelaide
item PURCELL, M. - University Of Adelaide
item GIBLIN-DAVIS, R. - University Of Florida
item THORNHILL, A. - Commonwealth Scientific And Industrial Research Organisation (CSIRO)
item YEATES, D. - Commonwealth Scientific And Industrial Research Organisation (CSIRO)

Submitted to: Biological Journal of the Linnean Society, London
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/14/2013
Publication Date: 3/12/2014
Citation: Nelson, L.A., Davies, K.A., Scheffer, S.J., Taylor, G.S., Purcell, M.F., Giblin-Davis, R.M., Thornhill, A.H., Yeates, D.K. 2014. An emerging example of tritrophic coevolution between flies (Diptera: Fergusoninidae) and nematodes (Nematoda: Neotylenchidae) on Myrtaceae host plants. Biological Journal of the Linnean Society, London. 111(4):699-718.

Interpretive Summary: Invasive species of weedy plants cause the U.S. and others hundreds of million dollars in direct losses and management costs associated with their control. The introduction of host-specific plant-feeding insects as biocontrol agents has proven to be a successful and environmentally benign approach to weed management. This study reviews the biology and host plant-specific relationships of plant-feeding flies that attack eucalypt species related to invasive paperbark trees. Challenges to a deeper understanding of the fly-eucalypt system are discussed. This information will be used by biocontrol scientists, taxonomists, and evolutionary biologists.

Technical 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 appears to be species-specific, and each mutualism in turn usually 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 such 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. This paper identifies the key questions to be addressed in this system, and proposes directions for future research. A framework for understanding the complex web of interactions in this system would include the identification and characterisation of each species in the plant/nematode/fly mutualism. Only a small fraction of the described Fergusonina species have complete records for corresponding myrtaceous host, gall type, fly larval morphology and a named Fergusobia nematode. Summaries of the known Fergusonina-Fergusobia species associations and gall type terminology are presented. Future research will profitably focus on (1) gall cecidogenesis, phenology and the classification of gall types, (2) the interaction between the fly larva and the nematode in the gall, and between the adult fly and the parasitic nematode, (3) the means by which the fly and nematode life cycles are coordinated and, (4) a targeted search of groups in the plant family Myrtaceae that have yet to have been identified as gall hosts. In order to adequately address the question of coevolution, the phylogenetic relationships of the host plants, the nematodes and the fergusoninid fly species need to be established and compared, most likely using multi-locus molecular datasets. Cophylogenies of the fly and nematode produced to date do not show strict congruence, and we explore some biological mechanisms that may explain this. We discuss the distribution of the Fergusoninidae/nematode mutualism with respect to recently derived phylogenies and divergence time estimation studies of the Diptera, Myrtaceae tribes and the genera of the Eucalypteae. These studies show that the fly family Fergusoninidae is a fraction of the age of the Myrtaceae, discounting the hypothesis of cospeciation and coradiation of the flies, nematode and the plants at the broadest level. However, cospeciation at more closely related levels in the phylogeny, such as sub-generic groups in Eucalyptus, is still possible.