A new obligate mutual pollination system involving Boronia (Rutaceae, Sapindales) and Heliozelidae (Adeloidea, Lepidoptera)

A project undertaken at the Walter and Eliza Hall Institute of Medical Research and supervised by Axel Kallies

Background

Obligate pollination mutualisms are rare, highly interdependent relationships between co-evolved insects and plants. The best known examples involve figs and fig wasps and yuccas and yucca moths, where the insects are required for pollination and plant survival, and the plant is the sole larval food source, hence essential for insect survival. These systems allow exploration of how co-evolving species interactions may arise and stabilise, and subsequently are exploited by "cheaters".

As part of our unpublished study of Australian Heliozelidae (a family of small, day-flying moths), we have identified many new genera and species. Unlike leaf-mining Palearctic and Nearctic Heliozelidae, many Australian species lay eggs into flowers, with larvae consuming seeds. One major clade of Heliozelidae appears to be tightly associated with the Rutaceae plant family. Within this clade, we have found a new genus with a unique pollen collecting structure on its abdomen, which appears to act as the obligate pollinator of Boronia megastigma and its close relatives. The Boronia hosts have other Heliozelidae associated with them that appear to play no role in pollination, but rather exploit or "cheat" the system.

The Boronia-Heliozelidae relationship is significant because unlike other mutualistic systems, Boronia species outside of the megastigma group appear to have generalist heliozelid pollinators, facilitating the exploration of the emergence of an obligate system. In addition, the small size of Boronia and their rapid development to maturity make them a tractable system to study. The goal of this project is to characterize the morphology and ecology of the pollinator and ‘cheater’ heliozelid moths, and scientifically describe them, thereby allowing their further study by ecologists and conservation groups.

Aims

Our aims for this project were:

  1. Produce a well-resolved phylogeny of the Heliozelidae family, and place the Australian Rutaceae-associated species within this context
  2. Examine Boronia species in the megastigma group to determine presence of pollinators and other associated Heliozelidae
  3. Use molecular techniques to resolve the evolutionary relationship of the pollinator species to other closely related Heliozelidae, allowing hypotheses about the obligate mutualism to be tested
  4. Formally describe the pollinator and 'cheater' species
Progress and findings

We produced a preliminary phylogeny of the Heliozelidae family based on four genes, which indicated that the Australian Rutaceae-associated species form a single (monophyletic) group. A robust backbone Heliozelidae phylogeny, based on over 500 genes from 46 taxa, has been completed, confirming the placement of the Rutaceae associated group within the family. We have identified heliozelid pollinators on most of the Boronia species in the megastigma group. Analysis of molecular data suggests pollinator species are highly host specific, providing further evidence of a pollination complex between Heliozelidae and Boronia. A preliminary phylogeny of the pollinators and closely related species indicates that the pollinator association may have a single origin. Significant progress has also been made on the taxonomic description of the pollinator species, including highly detailed SEM images of pollination structures.

Publications

Milla, L., Van Nieukerken, E. J., Vijverberg, R., Doorenweerd, C., Wilcox, S. A., Halsey, M., Young, D. A., Jones, T. M., Kallies, A. & Hilton, D. J. (2018). A preliminary molecular phylogeny of shield-bearer moths (Lepidoptera: Adeloidea: Heliozelidae) highlights rich undescribed diversity. Molecular Phylogenetics and Evolution, 120, 129-143.

Figure 1. Several species of heliozelid moths have formed pollinator associations with a group of Boronia, such as this putative new species on B. crenulata, both native to Western Australia.

Figure 2. Boronia megastigma is thought to be obligately pollinated by a single species of moth, a putative species of Heliozelidae.