Coevolutionary diversification and network structure of a specialized pollination mutualism on oceanic islands

Background/Question/Methods

Understanding the evolution and maintenance of ecological specialization is essential to understanding how lineages assemble into ecological networks.  In specialized, pollinating seed-predation mutualisms, such as between figs and fig wasps and yuccas and yucca moths, insects pollinate the flowers of their host plants but oviposit into the flowers so that their larvae may feed on developing seeds.  Unusually among non-symbiotic mutualisms, syntopic assemblages of these plants and insects exhibit strong reciprocal specialization and modularity.  Here, we examine the similar leafflower/leafflower moth system (Phyllanthaceae: Glochidion; Lepidoptera: Gracillariidae: Epicephala), focusing on the phylogenetics and network structure of ten species of leafflower trees and their pollinating moths on three oceanic islands (Tahiti, Moorea, and Huahine) in French Polynesia.  These are young islands (≤2.6 Ma) whose co-radiation of Glochidion and Epicephala should provide insights into the early stages of coevolutionary diversification.  Whereas the leafflower trees in this region are closely related and descend from a single colonization, the leafflower moths fall into two distantly related clades.  We ask whether moths in both clades coexist on the same host plant species or individual, and whether the networks on these islands show the same characteristics as those previously reported from congeners in continental Asia.

Results/Conclusions

We find that the Glochidion-Epicephala networks on these islands differ in several respects from each other and from their continental equivalents, although all networks show similar taxonomic diversity (3-5 Glochidion species and 2-4 Epicephala species).  Continental Glochidion-Epicephala networks show strong reciprocal specialization and modularity.  At a single location two Epicephala may coexist on one host species, but the reverse is never observed.  In contrast, the networks on all three islands show the sharing of multiple host plant species by a single Epicephala species, and on two of the three islands, the networks are not modular and show evidence of asymmetric specialization by Epicephala species.  On two of the three islands both moth clades coexist on the same host on one island (Huahine, Tahiti).  In contrast to previous work on this and similar systems, moths in each clade appear to have not diversified based on host plant species, although more recent divergence may be occurring that is not visible to mitochondrial and nuclear DNA sequences.  These findings suggest that closely related lineages can assemble into different realized topologies of interaction, and provide insights into the process of coevolutionary diversification and ecological sorting in these mutualisms.