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

Abstract

A challenge for coevolutionary theory is how different types of interaction influence the diversification of coevolving clades. Reciprocal specialization is characteristic of certain coevolving, mutualistic interactions, but whether this specialization seen in ecological time constrains changes in patterns of interaction over evolutionary time remains unclear. Here, we examine the co-radiation of Glochidion trees (Phyllanthaceae: Phyllanthus s. l.) and pollinating, seed-predatory Epicephala moths (Lepidoptera: Gracillariidae) on young (mostly later than 5 Ma) oceanic islands in southeastern Polynesia. Epicephala are the sole known pollinators of Glochidion trees, and show extreme reciprocal specialization in continental Asia. We find that Glochidion and Epicephala diversified across these islands through repeated, non-congruent colonizations, and that one recently colonizing Epicephala lineage has spread across 12 host species in three archipelagos in less than 1 Myr. These results indicate that reciprocal specialization and coadaptation do not prevent dramatic changes in associations between intimately associated taxa over short evolutionary time scales. Not only are these host associations more dynamic than previously recognized, but these changes in patterns of interaction may play an important role in the diversification of coevolving taxa.

Pollinator sharing and gene flow among closely related sympatric dioecious fig taxa

“…The evolutionary relationships between plant species and their obligate pollinators vary among different obligate pollination systems (e.g. Epicephala-Phyllantheae [52]; euglossine bees-fragrance orchids [48]; sexually deceptive orchids [11]). However, plants in all such systems mainly depend on specific floral volatiles for establishing relatively strict but not absolute pollinator specificity (thus pre-zygotic isolation) among sympatric plant species [6,7,10,24].…”

A Novel, Enigmatic Basal Leafflower Moth Lineage Pollinating a Derived Leafflower Host Illustrates the Dynamics of Host Shifts, Partner Replacement, and Apparent Coadaptation in Intimate Mutualisms

“…Consequently, the extent to which these interactions are phylogenetically constrained over evolutionary timescales has been of interest since the days of the earliest cophylogenetic analyses (Chenuil and McKey 1996; Herre et al 1996; Itino et al 2001; Lopez-Vaamonde et al 2001; Piercey-Normore and DePriest 2001; Weiblen 2001; Kawakita et al 2004; Quek et al 2004; Kawakita and Kato 2009; Althoff et al 2012; Cruaud et al 2012 a ; Hembry et al 2013; Chomicki et al 2015; Yang et al 2015). It is clear that in many cases, mutualisms between eukaryotic hosts and microbial endosymbionts are vertically transmitted and consequently show significant phylogenetic congruence (e.g., Moran et al 1993; Baumann and Baumann 2005; Urban and Cryan 2012).…”

Four new species of Epicephala Meyrick, 1880 (Lepidoptera, Gracillariidae) associated with two species of Glochidion (Phyllanthaceae) from Hainan Island in China

“…In China, thirteen species have been recorded prior to this study (Meyrick 1935; Kendrick 2005; Hu et al 2011a, b; Zhang et al 2012b; Li and Yang 2015; Wang and Li 2015; Yang and Li 2015). But there are still a large number of undescribed species of Epicephala , especially in tropical areas (Kawakita et al 2004; Kawakita and Kato 2006, 2009; Hembry et al 2012, 2013). …”