Phylogeny and host relationships of the Australian gall-inducing fly Fergusonina Malloch (Diptera: Fergusoninidae)

Abstract

Fergusoninidae is a monogeneric family of mainly Australian flies. In a unique obligate mutualism with a nematode, these flies induce galls on plants in the family Myrtaceae, and have been recorded on seven genera of host plants, most commonly on the eucalypts. Most host plants are associated with multiple species of Fergusonina, usually galling different sites on the plant. Despite the abundance and diversity of Fergusoninidae and its tight association with Australia’s most iconic flora, the host specificity and coevolutionary relationships of Fergusonina with its plant hosts have not previously been examined in depth. I used a phylogenetic approach based on mitochondrial COI to examine the evolutionary relationships between Fergusonina species and their plant hosts, initially performing a Bayesian analysis of 41 putative species on flies from Eucalyptus plant hosts. This analysis revealed well-supported lineages of flies characterised by larval morphology and gall type, usually from the same plant host subgenus. The deeper phylogenetic relationships between groups of species remained unclear, so I performed a further analysis of an expanded dataset including flies from four host genera, using separate and concatenated COI and nuclear CAD sequences. Having disparate evolutionary time scales, Fergusonina and their hosts cannot have codiverged early in the history of Myrtaceae, but current fly-plant host specificity suggested that there may be cospeciation at finer taxonomic levels. A fine-scale analysis of vi flies collected from a clade of ten Eucalyptus species explored the plant-fly coevolutionary relationships in three clades of flies from different sites of the host plant: flower buds, leaf blades and vegetative shoot buds. The degree of host specificity displayed by the three fly groups varied markedly, with flower bud gallers exhibiting the most cophylogenetic history, and leaf blade gallers the least. These results suggest that host switching occurred often in the history of Fergusonina and Myrtaceae. I compared molecular, morphological and ecological criteria for determining species limits, including a number of molecular species delimitation models. Delimiting species using a 2% pairwise distance was most consistent with other data such as larval and adult morphology, host and gall site. However, molecular methods were not adequate to clarify some ambiguous species limits, highlighting the need to integrate multiple criteria when identifying species in this group. Over the course of the study, I discovered around 95 unrecorded host plant/gall site associations, indicating that the potential number of species in this family is very large. The definable morphological and ecological differences among the lineages of Fergusonina, supported by molecular evidence, argue for a revision of the genus along these lines. The type species for Fergusonina, collected in Sydney in 1924, is in poor condition and is not identifiable; there are no records of its host, gall type or larval morphology, and I could not extract and DNA from it. A neotype will need to replace the existing holotype, or the type species assigned to a probable group. After a comparison of morphological characters I concluded that the type species is likely to belong to a group associated with the host genus Corymbia.