Repeated colonization of remote islands by specialized mutualists

Abstract

Mutualisms are ubiquitous in nature, but constraints imposed by specialization may limit their ability to colonize novel environments synchronously. The ability of mutualisms to reassemble following disturbance is central to understanding their response to global change. Here, we demonstrate that a highly specialized pollination mutualism considered to be obligate (Phyllanthaceae: Glochidion ; Lepidoptera: Gracillariidae: Epicephala ) has colonized some of the world's most isolated archipelagoes, and we record, to our knowledge, for the first time the presence of Epicephala moths from 19 host Glochidion species on 17 islands in the Pacific Ocean. Our findings appear to offer a remarkable example of mutualism persistence in an insect–plant interaction characterized by reciprocal specialization and mutual dependence. These findings also appear to contradict the island biogeography paradigm that taxa with specialized biotic interactions are unlikely to colonize oceanic islands.

Diversification through multitrait evolution in a coevolving interaction

“…It is likely, though, that more plants are pollinated by floral parasites than is currently known. For example, only within the past decade has pollination by insects during oviposition been discovered in the Phyllanthaceae in the tropical Pacific, involving possibly hundreds of plant species, and discovery of similar pollination mutualisms within this and other plant families continues (6,11,30,31).…”

“…Pollination by floral parasites has arisen and diversified repeatedly among plant lineages that are common components of terrestrial communities worldwide (4)(5)(6)(7)(8)(9). Examples include yuccas in North America, figs in tropical environments, globeflowers (Trollius; Ranunculaceae) in boreal ecosystems, and leafflower (Glochidion; Phyllanthaceae) trees in Asia and the Pacific islands (7,(10)(11)(12). The pollinators have coradiated with the plants, but often in ways that reflect the complex historical biogeography of these interactions (13,14).…”

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

“…Species specificity is very high and mediated by floral odour [30,31]. The biological intimacy of the mutualism [24], co-adapted traits of the associates [24,31], mutual dependency of the two clades for their life cycles [24,29,33] and convergent evolution of Glochidion floral morphology with that of other Epicephalapollinated leafflowers [34] all indicate that Glochidion and Epicephala have coevolved, but do not indicate how they diversified or how their patterns of interaction have changed over time. Previous analyses have found that phylogenies of Glochidion and its clade of Epicephala on continents and west Pacific islands are significantly but not exactly congruent [26], and in one case two distantly related Epicephala species coexist sympatrically on one Glochidion host species [30].…”

“…We dissected genitalia of the male southeastern Polynesian Epicephala (all of which were endemic [33] and, with one exception [61], undescribed) to determine whether morphology was consistent with the patterns revealed by molecular phylogenetic analysis.…”

“…We examine the co-radiation of 24 described species of Glochidion and their Epicephala pollinators in southeastern Polynesia (Cook Islands, French Polynesia and Pitcairn Islands; electronic supplementary material, figure S1) [33,[35][36][37], which is likely to represent a recent, in situ radiation resulting from a limited number of colonization events. The high islands of southeastern Polynesia comprise a series of archipelagos (the southern Cook, Society, Austral, Tuamotu, Marquesas, Gambier and Pitcairn islands; figure 1), all of which were formed by rspb.royalsocietypublishing.org Proc R Soc B 280: 20130361 midplate volcanoes under the Pacific plate [38].…”