Reversal of mutualism in a leafflower-leafflower moth association: the possible driving role of a third-party partner

Abstract

A major goal in the study of mutualism is to understand how co-operation is maintained when mutualism may potentially turn into parasitism. Although certain mechanisms facilitate the persistence of mutualism, parasitic species have repeatedly evolved from mutualistic ancestors. However, documented examples of mutualism reversals are still rare. Leafflowers (Phyllantheae; Phyllanthaceae) include approximately 500 species that engage in obligate mutualism with leafflower moths (Epicephala; Gracillariidae), which actively pollinate flowers, and whose larvae feed on the resulting seeds. We found that the Taiwanese population of the Phyllanthus reticulatus species complex was associated with six sympatric Epicephala species, of which three were derived parasites that induced gall formation on flowers/buds and produced no seeds. Notably, two parasitic species have retained mutualistic pollination behaviour, suggesting that the parasitism was likely not selected for to reduce the cost of mutualism. We propose that the galling habit evolved as an adaptation to escape parasitism by a specialized braconid wasp. The tough gall produced by one species was almost free of braconid parasitism, and the swollen gall induced by the other species probably prevents attack as a result of the larger airspace inside the gall. Our findings suggest that the presence of a third-party partner can greatly influence the evolutionary fate of mutualisms, regardless of whether the pairwise interaction continues to favour co-operation.

A non‐pollinating moth inflicts higher seed predation than two co‐pollinators in an obligate pollination mutualism

“…One of the wasp species, Bracon sp. 1, was closely related to another Bracon species that attacks Epicephala in the fruits of Phyllanthus reticulatus (Kawakita et al ., ). Phyllanthus reticulatus and B. oblongifolia are only distantly related (Kawakita & Kato, ) and their pollinating Epicephala species are also thought not to be closely related (Kawakita et al ., ).…”

“…taken from the fruits of Phyllanthus reticulatus Poir. in Taiwan (Phyllanthaceae), where it occurs as a parasitoid of pollinating Epicephala species (Kawakita et al, 2015).…”

“…A closely related Bracon species (Bracon sp. AK-2015-3) taken from the fruits of Phyllanthus reticulatus by a previous study (Kawakita, Mochizuki & Kato, 2015) was included for comparison.…”

“…1, was closely related to another Bracon species that attacks Epicephala in the fruits of Phyllanthus reticulatus (Kawakita et al, 2015). Phyllanthus reticulatus and B. oblongifolia are only distantly related (Kawakita & Kato, 2009) and their pollinating Epicephala species are also thought not to be closely related (Kawakita et al, 2015). As such, it would be interesting to consider the patterns of co-speciation and host use in Bracon and other parasitoids within the Phyllantheae and contrast this with pollinators and seed parasites.…”

Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown

“…Even mutualisms that have become highly dependent over millions of years of co-evolution, have broken down in some occasions. This is the case, for example, when free-living fungi evolved from a previously lichenised lifestyle, or when parasitic moths evolved from pollinating ancestors (20–22). Yet, while we have a good understanding of why mutualistic cooperation is favoured, we lack a general understanding of the drivers of these evolutionary breakdowns of mutualisms.…”