An Extreme Case of Plant–Insect Codiversification: Figs and Fig-Pollinating Wasps

Abstract

It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant–insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant–insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.]

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

“…Phylogenetic relationships among pollinators of five focal fig taxa detected from the phylogeny based on exclusively de novo sequences (electronic supplementary material, figure S3) were confirmed with the super-phylogeny of all Ceratosolen species recorded in GenBank (electronic supplementary material, figure S1), and the relationship was also congruent with the recent publication of wasp phylogeny [26]. At least six monophyletic clades of focal pollinators were detected with both the de novo sequences and sequences downloaded from GenBank (electronic supplementary material, figure S1; table 1).…”

“…Each individual would be assigned as an immigrant from a specific population, a non-migrant, or an offspring of immigrant and non-migrant (hybrids) based on its genotype. [26,37] and morphological classification [34]. The procedure herein follows that in Xu et al's work [37].…”

“…The 87 de novo sequenced sequences in this study were also included. Two Ceratosolen species-C. vissali (host F. theophrastoides) and C. acutatus (host F. vogeliana), which are taxonomically distantly related with C. emarginatus and C. gravelyi in a recent super wasp phylogeny [26]-were removed as their aligned sequence are too short (less than 400 bp). One to 10 sequences of each non-focal Ceratosolen species were maintained to achieve each species representation.…”

Cross-bracing uncalibrated nodes in molecular dating improves congruence of fossil and molecular age estimates

“…Grounded upon the tenet that the amount of time elapsed since the last common ancestor of two homologous sequences is statistically proportional to the number of differences between sequences, molecular dating has become an invaluable tool for hypothesis testing in evolutionary biology [2][3][4]. Numerous evolutionary processes are informed by inference of molecular divergence times, such as quantifying major historical shifts in cladogenetic rate [5,6], falsifying biogeographic hypotheses [7], or identifying co-diversification events in diverse, symbiotic lineages [8].…”

First record of a non-pollinating fig wasp (Hymenoptera: Sycophaginae) from Dominican amber, with estimation of the size of its host figs

“…Fig trees and their pollinating wasps probably arose about 75 million years ago in the Cretaceous period (Cruaud et al 2012) and subsequently diversified to generate the 750+ fig tree species and more than 1000 pollinator species present today (Berg and Corner 2005). (Galil and Eisikowitch 1968).…”