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Out of Australia and back again: the world-wide historical biogeography of non-pollinating fig wasps (Hymenoptera: Sycophaginae)

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Abstract Aim 

Figs (Ficus, Moraceae) are exploited by rich communities of often host-specific phytophagous wasps. Among them, gall-inducing Sycophaginae (Hymenoptera, Chalcidoidea) may share a common history with Ficus and their mutualistic pollinators (Agaonidae). We investigate here, for the first time, the phylogeny and biogeographical history of Sycophaginae and compare the timing of radiation and dispersion of major clades with available data on Ficus and fig pollinators. Reconstructing the history of their host colonization and association over space and time is central to understanding how fig wasp communities were assembled. Location 

World-wide. Methods 

Maximum likelihood and Bayesian analyses were conducted on 4267 bp of mitochondrial and nuclear DNA to produce a phylogeny of all genera of Sycophaginae. Two relaxed clock methods with or without rate autocorrelation were used for date estimation. Analyses of ancestral area were also conducted to investigate the geographical origin of the Sycophaginae. Results 

The phylogeny is well resolved and supported. Our data suggest a post-Gondwanan origin for the Sycophaginae (50–40 Ma) and two independent out-of-Australia dispersal events to continental Asia. Given palaeoclimatic and palaeogeographic records, the following scenario appears the most likely. The ancestor of Idarnes+Apocryptophagus migrated to Greater India through the Ninetyeast Ridge (40–30 Ma). The ancestor of Anidarnes+Conidarnes dispersed later via Sundaland (25–20 Ma). Idarnes and Anidarnes subsequently reached the New World via the North Atlantic land bridges during the Late Oligocene Warming Event. Apocryptophagus reached Africa c. 20 Ma via the Arabic corridors and returned to Australasia following the expansion of Sundaland tropical forests (20–10 Ma). Main conclusions 

Sycophaginae probably invaded the fig microcosm in Australia c. 50–40 Ma after the origin of their host plant. Once associated with figs, they dispersed out of Australia and radiated together with their host fig and associated pollinator through the tropics. We recorded a good coincidence of timing between dispersal events of Sycophaginae and continental connections. Furthermore, fruit pigeons that disperse figs probably spread out of Australasia through the Indian Ocean via the Ninetyeast Ridge c. 38 Ma. Therefore, our study highlights the potential for combining molecular phylogenetics with multiple methods of dating of interacting groups to reconstruct the historical biogeography of plant–herbivore associations.
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Keywords: Biogeography; Ficus; Ninetyeast Ridge; dispersal; divergence times; fig wasps; gall-inducing insects; phylogeny

Document Type: Research Article

Affiliations: 1: INRA-UMR Centre de Biologie et de Gestion des Populations, CBGP, (INRA/IRD/CIRAD/Montpellier SupAgro), Campus International de Baillarguet, CS 30016, 34988 Montferrier-sur Lez, France 2: Génoscope, Centre National de Séquençage, 2 Rue Gaston Crémieux, F-91057 Evry, France 3: Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, 88 Xuefu Road, 650223 Kunming, Yunnan, China 4: Entomology Laboratory, Zoology Division (Museum Zoologicum Bogoriense), Center Research for Biology, LIPI, Gedung Widyasatwaloka Jl. Raya Jakarta-Bogor, Km 46, Cobinong 16911, Bogor, Indonesia 5: Depto de Biologia/FFCLRP-USP, Av. Bandeirantes, 3900, 14040-901 – Ribeirão Preto, SP, Brazil 6: CNRS – UMR Centre d’Ecologie Fonctionnelle et Evolutive, CEFE, 1919 Route de Mende, 34293 Montpellier Cedex 5, France 7: INRA, UMR BioGeCo., 69 Route d’Arcachon, F-33612 Cestas Cedex, France

Publication date: 2011-02-01

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