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

Abstract

Coevolved mutualisms often exhibit high levels of partner specificity. Obligate pollination mutualisms, such as the fig -fig wasp and yucca -yucca moth systems, represent remarkable examples of such highly species-specific associations; however, the evolutionary processes underlying these patterns are poorly understood. The prevailing hypothesis suggests that the high degree of specificity in pollinating seed parasites is the fortuitous result of specialization in their ancestors because these insects are derived from endophytic herbivores that are themselves highly host-specific. Conversely, we show that in the Glochidion -Epicephala obligate pollination mutualism, pollinators are more host-specific than are closely related endophytic leaf-feeding taxa, which co-occur with Epicephala on the same Glochidion hosts. This difference is probably not because of shifts in larval diet (i.e. from leaf-to seed-feeding), because seed-eating lepidopterans other than Epicephala do not show the same degree of host specificity as Epicephala. Species of a tentative sister group of Epicephala each attack several distantly related plants, suggesting that the evolution of strict host specificity is tied to the evolution of pollinator habit. These results suggest that mutualists can attain higher host specificity than that of their parasitic ancestors and that coevolutionary selection can be a strong promoter of extreme reciprocal specialization in mutualisms.

Non-congruent colonizations and diversification in a coevolving pollination mutualism on oceanic islands

“…Thus, it is possible that at a fine scale, closely related species of Glochidion and their Epicephala pollinators diversify in a manner that results in phylogenetic incongruence, but that still produces some detectable congruence at larger phylogenetic scales. Similar patterns are apparent in fig wasps [16,22,27,78] and yucca moths [16]. These results underscore that we should not necessarily expect coevolving clades undergoing diversification to show phylogenetic congruence, even in highly specialized mutualisms [4,79] (but see [80]).…”

“…figs, leafflowers; but see [15]). It is not known whether the factors that promote high reciprocal specialization in these mutualisms (which may include coevolutionary selection [27], ancestral specialization [6] or pollinator-pollinator competition [28]) additionally constrain diversification and changes in the patterns of interaction over evolutionary time scales. These factors might constrain taxa to cospeciate (or phylogenetically track one another) over short evolutionary time scales, with host-shifts being rare events.…”

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

“…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. In this way, we may learn more about the factors that affect host specificity in mutualistic, parasitic and antagonistic interactions, as has previously been studied in Glochidion (Kawakita et al ., ).…”

Both plant genotype and herbivory shape aspen endophyte communities

“…Under the assumption that mutualism favours higher host specificity compared to antagonism (Kawakita et al 2010), network analyses may suggest which qualities exist in a bipartite community (Bascompte et al 2006). We found that the mycobiome that had formed in the leaves after herbivory was less associated with the genetic background of the host, which thus suggests that the relationship between these young aspen trees and the endophytic mycobiome developed into an increasingly common and potentially antagonistic structure (Bascompte et al 2006).…”