Repeated independent evolution of obligate pollination mutualism in the Phyllantheae– Epicephala association

Abstract

The well-known fig-fig wasp and yucca-yucca moth mutualisms are classic examples of obligate mutualisms that have been shaped by millions of years of coevolution. Pollination systems involving obligate seed parasites are only expected to evolve under rare circumstances where their positive effects are not swamped by abundant co-pollinators and heavy costs resulting from seed destruction. Here, we show that, in Phyllantheae, specialization to pollination by Epicephala moths evolved at least five times, involving more than 500 Phyllantheae species in this obligate association. Active pollination behaviour evolved once in Epicephala, 10-20 Myr after the initial divergence of their host plants. The pollinating Epicephala moths thus radiated on an already-diverged host lineage and successively colonized new Phyllantheae hosts, thereby giving rise to repeated independent evolution of the specialized pollination system in Phyllantheae. The present evolutionary success of this association rests entirely upon active pollination by Epicephala, making this a distinct example of an evolutionary key innovation. Overall, our findings provide a clear empirical demonstration of how a combination of evolutionary innovation and partner shifts facilitates the spread of mutualism in a coevolving species interaction.

Mutualism favours higher host specificity than does antagonism in plant–herbivore interaction

“…The most basal lineage of Epicephala is a non-pollinator that attacks the seeds of Flueggea, a close relative of Glochidion within the tribe Phyllantheae. However, this species is currently known only from Flueggea suffruticosa in southwestern Japan (Kawakita & Kato 2009), where there are no other cooccurring Flueggea species. Also, a derived clade of Epicephala has secondarily lost the pollinating habit, and currently there are three species that are each specific to a single Phyllanthus host (Kawakita & Kato 2009).…”

“…However, this species is currently known only from Flueggea suffruticosa in southwestern Japan (Kawakita & Kato 2009), where there are no other cooccurring Flueggea species. Also, a derived clade of Epicephala has secondarily lost the pollinating habit, and currently there are three species that are each specific to a single Phyllanthus host (Kawakita & Kato 2009). However, closely related Phyllanthus hosts are rarely available within the same population, which precludes a direct comparison of host specificity with pollinating Epicephala in this case as well.…”

“…Although the use of different host plant families in Epicephala and Cuphodes may make direct comparison difficult, available evidence suggests that Cuphodes species exhibit much broader host ranges than do the species of Epicephala. For example, C. wisteriae uses Wisteria and Millettia, which are distantly related genera within Fabaceae, having diverged at least 50 Ma (Lavin et al 2005), whereas the age of the Glochidion crown group is estimated to be less than 10 Ma (Kawakita & Kato 2009). Similarly, Cuphodes sp.…”

“…Currently, an estimated 500 species of Phyllantheae plants exist that are pollinated by the ovipositing females of Epicephala moths (Kawakita & Kato 2009;Kawakita 2010). Among them are plants of the genus Glochidion, which is the largest radiation and comprises more than 300 species distributed throughout the Asian -Australian tropics (Govaerts et al 2000).…”

Phylogenetic reconstruction prompts taxonomic changes in <I>Sauropus</I>, <I>Synostemon</I> and <I>Breynia</I> (<I>Phyllanthaceae</I> tribe <I>Phyllantheae</I>)

“…Because of these differences in morphology Sauropus and Breynia were always kept separate. The Epicephala pollination originated several times independently in the Phyllantheae (Kawakita & Kato 2009). …”