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Specific, Non-Nutritional Association Between an Ascomycete Fungus and Allomerus Plant-Ants

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Specific, Non-Nutritional Association Between an Ascomycete Fungus and Allomerus Plant-Ants Downloaded from rsbl.royalsocietypublishing.org on May 12, 2011 Biol. Lett. (2011) 7, 475–479 symbiosis with basidiomycetes in which both partners doi:10.1098/rsbl.2010.0920 are codependent, and that shows their reciprocal Published online 17 November 2010 specializations and codispersal [4–6]. Besides such Population ecology cultivation of fungal crops, few non-food associations between ants and fungi have been reported to date in which fungi occur in ant constructions or inside the Specific, non-nutritional domatia of ant-plants [7–12]. These occurrences of fungi in the constructions or inside the domatia are association between an not the result of the growth of opportunistic species, but of specific interactions [9,12]. These studies also ascomycete fungus and suggest that the active maintenance and management Allomerus plant-ants of fungi by ants for non-nutritional purposes may be more widespread than currently assumed [13]. Mario X. Ruiz-Gonza´lez1,2,†, Pierre-Jean G. Male´ 1,2, Here we address this issue in Neotropical plant-ants Ce´line Leroy3, Alain Dejean3, Herve´ Gryta1,2, of the genus Allomerus, associated with the myrmeco- Patricia Jargeat1,2, Ange´lique Quilichini3 phytes Hirtella physophora Martius & Zuccharini and and Je´roˆ me Orivel3,* Cordia nodosa Lamarck. To ambush prey, these ants build galleries under the stems of their host plants 1UPS; Laboratoire Evolution et Diversite´ Biologique, Universite´ de Toulouse, 118 route de Narbonne, 31062 Toulouse, France using trichomes that they assemble into a frame on 2CNRS; Laboratoire Evolution et Diversite´ Biologique, 31062 Toulouse, which then grows a fungal mycelium that reinforces France the structure [8]. It has not yet been demonstrated, 3CNRS; UMR Ecologie des Foreˆts de Guyane (UMR-CNRS 8172), Campus Agronomique, 97379 Kourou cedex, France however, whether the ants cultivate the fungi or if the *Author for correspondence ([email protected]). fungi are opportunistic species. We studied unknown †Present address: Instituto de Biologı´a Molecular y Celular de Plantas, aspects of the biology of this ant–fungus association, C.S.I.C.—U.P.V.C/ Ingeniero Fausto Elio s/n. 46022 Valencia, Spain. and both characterized and analysed the genetic popu- Ant–fungus associations are well known from lation structure of the fungi from the galleries and of attine ants, whose nutrition is based on a symbio- their associated ants (Allomerus decemarticulatus Mayr sis with basidiomycete fungi. Otherwise, only a and Allomerus octoarticulatus Mayr), sampled from few non-nutritional ant–fungus associations geographically distant areas within French Guiana. have been recorded to date. Here we focus on one of these associations involving Allomerus plant-ants that build galleried structures on their myrmecophytic hosts in order to ambush prey. We show that this association is not 2. MATERIAL AND METHODS opportunistic because the ants select from a (a) Sampling ants and traps monophyletic group of closely related fungal hap- Workers from 197 A. decemarticulatus and 43 A. octoarticulatus colo- lotypes of an ascomycete species from the order nies were sampled along with parts of their corresponding galleries Chaetothyriales that consistently grows on and from four areas in French Guiana between 2008 and 2009: Petit Saut, Sinnamary (0580402700 N, 5380302100 W; n ¼ 133/19 has been isolated from the galleries. Both the A. decemarticulatus/A. octoarticulatus colonies, respectively), ants’ behaviour and an analysis of the genetic Montagne des Singes (0580402000 N, 5284104300 W; n ¼ 26/6), population structure of the ants and the fungus Montagne de Kaw (0483203400 N, 5280901400 W; n ¼ 29/18) and argue for host specificity in this interaction. The Nouragues (0480501600 N, 5284004900 W; n ¼ 9/0). In addition, 18 ants’ behaviour reveals a major investment in domatia recently occupied by founding queens were dissected. manipulating, growing and cleaning the fungus. Such domatia were recognizable from the outside because the queen’s wings remained at the entrance and because the queen had A molecular analysis of the fungus demonstrates built a stockade to close the entrance. the widespread occurrence of one haplotype and Fungal samples were precultured in wet cotton and 15–30 single many other haplotypes with a lower occurrence, hyphae from the new mycelium were then cultured in solid yeast and as well as significant variation in the presence malt extract with glucose medium for 6–20 days (see details in the of these fungal haplotypes between areas and electronic supplementary material). ant species. Altogether, these results suggest that such an interaction might represent an as-yet undescribed type of specific association (b) Molecular and phylogenetic analysis of the between ants and fungus in which the ants culti- fungi and the ants vate fungal mycelia to strengthen their hunting The total DNA from all of the fungal and ant samples was extracted galleries. using a 10 per cent Chelex (BioRad) solution. A phylogenetic analy- sis was conducted on the entire internal transcribed spacer (ITS) Keywords: ant–fungus association; Cordia nodosa; region and the EF1a segment of the fungi, as well as the cytochrome Chaetothyriales; Hirtella physophora; myrmecophyte; c-oxydase (COI) and a segment of the cytochrome b gene of the population structure ants. In total, 114 fungal samples out of the 240 collected were successfully sequenced for both the ITS and EF1a segment (fungal isolation success of about 50%), and 91 ant colonies (69 A. decemarticulatus and 22 A. octoarticulatus) were successfully sequenced for both the COI and cytochrome b. Capronia pilosella and 1. INTRODUCTION Exophiala pisciphila were used as the fungal outgroup, and Insect fungiculture has evolved independently in four Monomorium subopacum, Diplorhoptrum sp., Solenopsis saevissima and orders of insects; i.e. ants, termites, ambrosia beetles Wasmannia auropunctata were used as the ant outgroup. Phylogenetic inferences were made using different criteria: maximum parsimony and gall midges [1–3]. In ants, species of the Attini (MP), neighbour-joining (NJ), maximum-likelihood (ML) and tribe are engaged in a highly coevolved nutritional Bayes. The genetic structure of the fungal variants detected in the cladograms was analysed using ARLEQUIN v. 3.1 [14] and the Electronic supplementary material is available at http://dx.doi.org/ AMOVA values for the FST were calculated after 10 000 permutations 10.1098/rsbl.2010.0920 or via http://rsbl.royalsocietypublishing.org. (see the electronic supplementary material). Received 1 October 2010 Accepted 28 October 2010 475 This journal is q 2010 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on May 12, 2011 476 M. X. Ruiz-Gonza´lez et al. Non-nutritional ant–fungus association (a) (b) (c) (d) (e) ( f ) (g) (h) Figure 1. Culture of the fungus and construction of the galleries. (a) Trichomes inside and outside a recently colonized doma- tium; (b) pellet made from plant material from the domatium close to the first eggs laid in the newly colonized domatium (arrow); (c) the founding queen scarifies the domatia wall (vertical arrow) where the first hyphae will grow in the suberous crust (horizontal arrow); (d) the growing fungus seals the entrance of the domatium until the first workers make an exit hole (arrow); (e) scaffold of trichomes; ( f ) highly scarified domatium; (g) the workers paste pellets made from the suberous crust of the domatia (arrows) on the frame of trichomes; and (h) the fungus grows from each of the pellets strengthening the galleries that the ants use as a trap (white arrow, trichomes; black arrow, pellets). Scale bar, 1 mm. 3. RESULTS The workers scarify the epidermis and mesophyll of Eleven out of the 18 founding queens recorded in the the inner walls of the domatia to prepare pellets of dissected domatia had only been installed for a very vegetal dough. These pellets are carried out of the short time, as they had laid few or no eggs. In all of domatia and pasted along the trichomes that form these 11 cases, a black pellet was clearly visible in the the future gallery (figure 1f–h). domatium wall or already pasted to the trichomes Forty-four fungal species present as spores were iso- that the queen had cut and piled at the entrance to lated directly from the galleries (table 1), but none of the domatium to close it (figure 1a). The pellet is them grow on these galleries unless the ants have made from plant material and the first hyphae grow been removed. Moreover, an examination of the infra- in the suberous crust. It remains, however, unknown buccal pellets of the workers demonstrated the active whether the queen brings the pellet and the fungus removal of fungal spores and contaminant hyphae from its mother colony or if it is already present in (M. X. Ruiz-Gonzalez 2009, unpublished results). By the new host plant (figure 1b–d). The seven remaining contrast, the mycelium of only one fungal species, a queens had already bred some larvae and pupae and sooty mould, was repeatedly noted in both the galleries the hyphae had entirely covered the domatia entrances. covering the plant stems and the domatia occupied by The first workers produced must excavate a tunnel the founding queens. This melanized fungus, with through this barrier to leave the domatia (figure 1d). elongated hyphae of 4.5–9 mm in diameter, consist- They then cut the trichomes along the stem, creating ently grew from the multi-replicated cultures (108 a path to new domatia and use the cut trichomes to and 31
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