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Open Access Research article

Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea)

Astrid Cruaud1*, Roula Jabbour-Zahab1, Gwenaëlle Genson1, Finn Kjellberg2, Noppol Kobmoo2, Simon van Noort3, Yang Da-Rong4, Peng Yan-Qiong4, Rosichon Ubaidillah5, Paul E Hanson6, Otilene Santos-Mattos7, Fernando HA Farache8, Rodrigo AS Pereira8, Carole Kerdelhué1 and Jean-Yves Rasplus1

Author 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 CNRS-UMR Centre d'Ecologie Fonctionnelle et Evolutive, CEFE, 1919 route de Mende, 34293 Montpellier Cedex 5, France

3 Natural History Division, South African Museum, Iziko Museums of Cape Town, PO Box 61, Cape Town 8000, South Africa

4 Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, 88 Xuefu Road, 650223 Kunming, Yunnan, China

5 Entomology Laboratory, Zoology Division (Museum Zoologicum Bogoriense). Center Research for Biology, LIPI, Gedung Widyasatwaloka Jl. Raya Jakarta-Bogor, Km 46, Cobinong 16911, Bogor, Indonesia

6 Escuela de Biología. Universidad de Costa Rica. A.P. 2060 San Pedro de Montes de Oca. San José, Costa Rica

7 Instituto Nacional de Pesquisa da Amazônia, av Andre Araujo 2936, 69060-001, Manaus, Amazonas, Brazil

8 Depto de Biologia/FFCLRP-USP, Av. Bandeirantes, 3900, 14040-901 - Ribeirão Preto, SP, Brazil

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BMC Evolutionary Biology 2011, 11:178  doi:10.1186/1471-2148-11-178

Published: 22 June 2011

Abstract

Background

Non-pollinating Sycophaginae (Hymenoptera, Chalcidoidea) form small communities within Urostigma and Sycomorus fig trees. The species show differences in galling habits and exhibit apterous, winged or dimorphic males. The large gall inducers oviposit early in syconium development and lay few eggs; the small gall inducers lay more eggs soon after pollination; the ostiolar gall-inducers enter the syconium to oviposit and the cleptoparasites oviposit in galls induced by other fig wasps. The systematics of the group remains unclear and only one phylogeny based on limited sampling has been published to date. Here we present an expanded phylogeny for sycophagine fig wasps including about 1.5 times the number of described species. We sequenced mitochondrial and nuclear markers (4.2 kb) on 73 species and 145 individuals and conducted maximum likelihood and Bayesian phylogenetic analyses. We then used this phylogeny to reconstruct the evolution of Sycophaginae life-history strategies and test if the presence of winged males and small brood size may be correlated.

Results

The resulting trees are well resolved and strongly supported. With the exception of Apocrytophagus, which is paraphyletic with respect to Sycophaga, all genera are monophyletic. The Sycophaginae are divided into three clades: (i) Eukoebelea; (ii) Pseudidarnes, Anidarnes and Conidarnes and (iii) Apocryptophagus, Sycophaga and Idarnes. The ancestral states for galling habits and male morphology remain ambiguous and our reconstructions show that the two traits are evolutionary labile.

Conclusions

The three main clades could be considered as tribes and we list some morphological characters that define them. The same biologies re-evolved several times independently, which make Sycophaginae an interesting model to test predictions on what factors will canalize the evolution of a particular biology. The ostiolar gall-inducers are the only monophyletic group. In 15 Myr, they evolved several morphological adaptations to enter the syconia that make them strongly divergent from their sister taxa. Sycophaginae appears to be another example where sexual selection on male mating opportunities favored winged males in species with small broods and wingless males in species with large broods. However, some species are exceptional in that they lay few eggs but exhibit apterous males, which we hypothesize could be due to other selective pressures selecting against the re-appearance of winged morphs.