Phylogenetics, historical biogeography, diversification and pollination ecology of Meiogyne (Annonaceae) : assessing hypotheses of trait- and environment- dependent transoceanic dispersal and floral mimicry

Abstract

Meiogyne Miq. is a woody genus (c. 34 spp.) from the early-divergent family Annonaceae and is widespread in Indomalaya and the Australasia-Pacific. The present molecular phylogenetic study expands taxon and DNA sampling, with 11 new nuclear DNA regions. The concatenated supermatrix yields well-resolved and strongly supported trees using maximum parsimony, maximum likelihood and Bayesian inference methods, providing a robust framework for testing macro-evolutionary hypotheses.

Meiogyne possesses contrasting fruit traits which may implicate macroevolutionary dispersal. I test this hypothesis using trait-dependent biogeographical models in BioGeoBEARS for two binary fruit traits: fruit colour (bright or dull), and monocarp width (narrow or wide). Trait-dependent model comparison suggests that narrow monocarps have promoted macroevolutionary dispersal, whilst a corresponding effect was not recovered for fruit colour. A correlation between arrow monocarp and bright fruit was identified. Both traits likely have co-evolved for bird dispersal, which likely drove long-distance dispersal (LDD) in Meiogyne, corroborating the importance of bird dispersal traits in promoting LDD in island taxa.

Abiotic factors are known to influence the diversification tempo of life. Meiogyne is a promising lineage for studying the effect of paleoclimate and sea level on diversification. A negative correlation was identified between sea-level fluctuation and diversification rate. The time-stratified biogeographical model suggested that sea-level fluctuation is associated with decreased LDD likelihood in the Australasia-Pacific and may explain the negative sea-level fluctuation diversification dependency. This sheds light on dispersal and diversification of island taxa that have experienced similar environmental stress.

A case of mushroom mimicry is reported here. Flowers of Meiogyne hirsuta, an undergrowth in the Australian wet tropics, emit a mushroom-like odour and have gill-like basal corrugations on the inner petals. The nitidulid Cychramus sp. was the sole effective pollinator, and was observed to consume stigmatic exudate and pollen. Oviposition was observed but larvae did not survive. With mushrooms being the only known brood site, oviposition of Cychramus sp. is indicative of cognitive misclassification, suggesting that the system is quasi-Batesian. Gas chromatography-mass spectrometry identified the C8 ketone 3-octanone as the most abundant volatile. The floral headspace was nested within the odour space of mushrooms in NMDS analyses, but did not overlap with Annonaceae flowers, suggesting advergence of the olfactory cue to mushrooms. This is the second case of mushroom mimicry in the rainforest dominant tree family Annonaceae.

A novel floral mimicry system of aerial litter is also reported. Meiogyne heteropetala produces maroon and mint- or bark-scented flowers that attract the aerial litter specialist erotylid Loberus sharpi. Eggs were found in living flowers while late instar larvae were observed in aerial withered petals. The brood site reward, however, was suboptimal as most petals fell to forest floor where larvae perish. Monoterpene and monoterpenoids dominated the floral headspace, with 1,8-cineole being the major component. Monoterpenes were also the major volatiles of co-occurring aerial litter and leafy twigs. Despite occupying neighbouring odour space, the floral headspaces did not overlap with aerial litter or leafy twigs, indicating imperfect mimicry. This is the first documentation of floral mimicry exploiting aerial litter as a model.