Diversification and spatial structuring in the mutualism between Ficus septica and its pollinating wasps in insular South East Asia Lillian Jennifer Rodriguez, Anthony Bain, Lien-Siang Chou, Lucie Conchou, Astrid Cruaud, Regielene Gonzales, Martine Hossaert-Mckey, Jean-Yves Rasplus, Hsy-Yu Tzeng, Finn Kjellberg To cite this version: Lillian Jennifer Rodriguez, Anthony Bain, Lien-Siang Chou, Lucie Conchou, Astrid Cruaud, et al.. Diversification and spatial structuring in the mutualism between Ficus septica and its pollinating wasps in insular South East Asia. BMC Evolutionary Biology, BioMed Central, 2017, 17, pp.207. 10.1186/s12862-017-1034-8. hal-01589491 HAL Id: hal-01589491 https://hal.sorbonne-universite.fr/hal-01589491 Submitted on 18 Sep 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Rodriguez et al. BMC Evolutionary Biology (2017) 17:207 DOI 10.1186/s12862-017-1034-8 RESEARCH ARTICLE Open Access Diversification and spatial structuring in the mutualism between Ficus septica and its pollinating wasps in insular South East Asia Lillian Jennifer Rodriguez1,2,3* , Anthony Bain4, Lien-Siang Chou4, Lucie Conchou2,5, Astrid Cruaud3, Regielene Gonzales1, Martine Hossaert-McKey2, Jean-Yves Rasplus3, Hsy-Yu Tzeng6 and Finn Kjellberg2 Abstract Background: Interspecific interactions have long been assumed to play an important role in diversification. Mutualistic interactions, such as nursery pollination mutualisms, have been proposed as good candidates for diversification through co-speciation because of their intricate nature. However, little is known about how speciation and diversification proceeds in emblematic nursery pollination systems such as figs and fig wasps. Here, we analyse diversification in connection with spatial structuring in the obligate mutualistic association between Ficus septica and its pollinating wasps throughout the Philippines and Taiwan. Results: Ceratosolen wasps pollinating F. septica are structured into a set of three vicariant black coloured species, and a fourth yellow coloured species whose distribution overlaps with those of the black species. However, two black pollinator species were found to co-occur on Lanyu island. Microsatellite data on F. septica indicates the presence of three gene pools that broadly mirrors the distribution of the three black clades. Moreover, receptive fig odours, the specific message used by pollinating wasps to locate their host tree, varied among locations. Conclusions: F. septica and its black pollinator clades exhibited similar geographic structuring. This could be due originally to geographic barriers leading to isolation, local adaptation, and finally co-structuring. Nevertheless, the co-occurrence of two black pollinator species on Lanyu island suggests that the parapatric distribution of the black clades is now maintained by the inability of migrating individuals of black pollinators to establish populations outside their range. On the other hand, the distribution of the yellow clade strongly suggests an initial case of character displacement followed by subsequent range extension: in our study system, phenotypic or microevolutionary plasticity has allowed the yellow clade to colonise hosts presenting distinct odours. Hence, while variation in receptive fig odours allows specificity in the interaction, this variation does not necessarily lead to coevolutionary plant-insect diversification. Globally, our results evidence evolutionary plasticity in the fig-fig wasp mutualism. This is the first documentation of the presence of two distinct processes in pollinating fig wasp diversification on a host species: the formation of vicariant species and the co-occurrence of other species over large parts of their ranges probably made possible by character displacement. Keywords: Biogeography, Ceratosolen, Mutualism, Philippines, Speciation * Correspondence: [email protected] 1Institute of Biology, University of the Philippines, Diliman, Quezon City, Philippines 2CEFE UMR 5175, CNRS—Université de Montpellier—Université Paul-Valéry Montpellier—EPHE, Montpellier, France Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Rodriguez et al. BMC Evolutionary Biology (2017) 17:207 Page 2 of 12 Background re-assembly, it has been generally assumed that establish- Interspecific interactions have long been assumed to play ment of obligate mutualisms in islands is highly unlikely an important role in diversification. Competitive coevolu- [15]. Nonetheless, existence of specialized mutualisms in tionary diversification among related species seems to be island complexes defies this assumption. Indeed, the common while mutualistic coevolutionary diversification Glochidion tree-Epicephala moth mutualism is present could be more exceptional [1]. Emblematic examples of throughout the tropical Pacific Islands [15]. Another allopatric speciation followed by competitive character example is the colonization of New Caledonia by section displacement in secondary contact zones include Anoles Oreosycea fig trees and their Dolichoris pollinators [16]. lizards in Caribbean islands [2], Darwin’s finches [3] and Although few, these studies show that dispersal and re- sticklebacks [4]. Nevertheless, despite numerous putative assembly of obligate mutualisms in islands is possible and cases, there are only few fully demonstrated examples of results in evolutionarily stable interactions. Such situations competitive character displacement [5]. allow analysing diversification patterns, some driven by Plants and their pollinators were proposed as models obstacles to gene flow and others by host shifts [15, 17]. that should be prone to mutualistic coevolutionary diver- The intricate island systems of South East Asia and sification, because pollinators disperse the gametes of the Australasia provide a diversity of situations in which Ficus plants whose flowers they visit [6]. Phylogenetic studies species have diversified, and also in which some Ficus spe- actually suggest that reciprocally-associated plant and pol- cies have spread out over numerous islands [18]. Neverthe- linator clades often undergo asynchronous diversification less, little is known about within-Ficus species diversification consistent with a model of plants diversifying in response among islands and about associated pollinating wasp diversi- to sensory biases of their pollinators (e.g., [7]). Further, fication. In insular systems, widespread Ficus species may be microevolutionary studies usually fail to test whether pol- pollinated by different, more or less cryptic species of wasps linators are evolving in response to the plants they visit. In in different parts of their range [17]. This is the case for nursery pollination systems, species-level specificity is Ficus septica, an insular fig species ranging from the Solo- often high, with most plant species usually locally polli- mon Islands to the Ryukyu Islands and throughout insular nated by only one or a few host-specific insect species. South East Asia [17]. Previous work on Ficus septica sug- This suggests that these mutualisms may coevolve. How- gested that coevolutionary diversification through competi- ever, little is known about how speciation and diversifica- tion could be at work among its pollinators, the Ceratosolen tion proceeds in emblematic nursery pollination systems bisulcatus species complex [19]. Further, published data sug- such as figs and fig wasps (but see [8]) or in Phyllantha- gests the presence of among-island variation in receptive fig ceae and their pollinating moths [9]. Because of the intri- odour in Ficus septica, i.e. variation in the main message cate nature of these interactions, they have often been used by the wasps to locate their hosts (compare [19, 20]). proposed as good candidates for diversification through Our goal in this study was to describe the general pattern co-speciation. However, comparing Ficus and their pollin- of diversification within the Ficus septica-pollinating wasps ating wasp phylogenies has shown that only 2/3 of the system and to demonstrate that it is consistent with the nodes are coevolved, and this is the most extreme ex- hypotheses (1) that geographic differentiation of receptive ample documented today of plant-insect codiversification fig odours within Ficus septica,thoughpresent,isnota [10]. At least in some of these systems,