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Fungal sex as a private matter: odour signals in a specialized pollination‐like insect–fungus mutualism

2008; Wiley; Volume: 178; Issue: 2 Linguagem: Inglês

10.1111/j.1469-8137.2008.02428.x

1469-8137

Martine Hossaert‐McKey, Doyle McKey, Laurent Dormont,

Forest Insect Ecology and Management

New PhytologistVolume 178, Issue 2 p. 225-227 Free Access Fungal sex as a private matter: odour signals in a specialized pollination-like insect–fungus mutualism Martine Hossaert-McKey, Martine Hossaert-McKey Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), UMR CNRS 5175, 1919 route de Mende, F-34293 Montpellier Cedex 5, France (*Author for correspondence: tel +33 4 67 61 32 30; fax +33 4 67 41 21 38; email [email protected])Search for more papers by this author* Doyle McKey, Doyle McKey Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), UMR CNRS 5175, 1919 route de Mende, F-34293 Montpellier Cedex 5, France (*Author for correspondence: tel +33 4 67 61 32 30; fax +33 4 67 41 21 38; email [email protected])Search for more papers by this authorLaurent Dormont, Laurent Dormont Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), UMR CNRS 5175, 1919 route de Mende, F-34293 Montpellier Cedex 5, France (*Author for correspondence: tel +33 4 67 61 32 30; fax +33 4 67 41 21 38; email [email protected])Search for more papers by this author Martine Hossaert-McKey, Martine Hossaert-McKey Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), UMR CNRS 5175, 1919 route de Mende, F-34293 Montpellier Cedex 5, France (*Author for correspondence: tel +33 4 67 61 32 30; fax +33 4 67 41 21 38; email [email protected])Search for more papers by this author* Doyle McKey, Doyle McKey Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), UMR CNRS 5175, 1919 route de Mende, F-34293 Montpellier Cedex 5, France (*Author for correspondence: tel +33 4 67 61 32 30; fax +33 4 67 41 21 38; email [email protected])Search for more papers by this authorLaurent Dormont, Laurent Dormont Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), UMR CNRS 5175, 1919 route de Mende, F-34293 Montpellier Cedex 5, France (*Author for correspondence: tel +33 4 67 61 32 30; fax +33 4 67 41 21 38; email [email protected])Search for more papers by this author First published: 26 March 2008 https://doi.org/10.1111/j.1469-8137.2008.02428.xCitations: 3AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Volatile organic compounds (VOCs) are well known to play many ecological roles in insect–plant interactions (Pichersky & Gershenzon, 2002), both mutualistic and antagonistic, and these range from loose, diffuse interactions to highly specialized symbioses. For many kinds of interactions (for example, among mutualisms, plant–pollinator interactions) the great diversity of compounds involved has also been well documented (Knudsen et al., 2006). By contrast, few studies have examined the role of VOCs in interactions between insects and fungi. These include cases in which phytophagous or parasitoid insects respond to common fungal volatiles emitted by infected plants, being either attracted (Honda et al., 1988) or repelled (Steiner et al., 2007), depending on whether the effect of fungal infection on their habitat quality is positive or negative. The impact of odour production on the fitness of the fungus itself is unclear. Other studies concern interactions in which the fungus appears to have more at stake, with more direct selection on the traits of their odour signals. These include, most notably, floral mimicry systems in which plant-pathogenic fungi produce 'pseudoflowers' that attract diverse assemblages of insect species, ensuring the transfer of gametes in obligately outcrossing fungi and sometimes conferring 'nectar' rewards to insect visitors (Raguso & Roy, 1998; Naef et al., 2002). In such systems, as in plant–insect pollination mutualisms, selection might often favour specialization of attraction to increase pollinator constancy and the efficiency of gamete transfer. Insects have been associated with fungi as long as they have been with plants, and specialized and specific insect-mediated fungal 'pollination' systems have indeed evolved. It would be surprising if VOCs did not play roles in specific attraction in such systems, as they do in highly specialized insect–flower interactions. In this issue of New Phytologist (pp. 401–411), Steinebrunner et al. document the role of VOCs in an obligate symbiotic insect–fungus mutualism, in which specific insects are essential for fungal sex. In this system, as in highly specific symbiotic pollination mutualisms like those involving Yucca and Ficus, VOCs play an important role in the specific attraction of the 'pollinator' insects (Grison-Pigéet al., 2002a; Svensson et al., 2006). 'In the Epichloë–Botanophila mutualism the few compounds present are highly unusual substances.' Steinebrunner et al. studied the interaction between Epichloë fungi (Ascomycota) and Botanophila flies (Anthomyiidae). Epichloë live as endophytes in intercellular spaces of pooid grasses. On flowering tillers of the host, they produce stromata, reproductive structures in which fungal tissue overgrows the developing tillers. The stroma produces spermatia (fungal male gametes) and, after mating, produces meiotic spores that are disseminated to other hosts. Because the fungus is self-incompatible and thus obligately outcrossing, its reproduction depends on the transport of spermatia to an individual of the opposite mating type (Schardl, 1996). The usual vectors are Botanophila flies. Adult flies are attracted to the stromata, where they consume spermatia. After flying to another stroma, they defecate spermatia intact, actively spread them over the stroma and lay one or more eggs. The developing larvae then eat stromata fungal tissue. Flies are presumed to benefit from active 'pollination' as better fertilization results in more food for larvae. Larvae have been hypothesized to be dependent on fungal sporulation organs (perithecia), produced after cross-fertilization, as their sole food source, but, as the authors note, this hypothesis has been called into question and the larvae of at least some Botanophila spp. can complete development on unfertilized stromata (Rao et al., 2005). While the two genera are linked in obligate symbiosis, the degree of species specificity of Epichloë–Botanophila interactions is unclear. At broad geographic scales, species specificity is limited. There is also no evidence for co-evolution: related species are not associated with related hosts (Leuchtmann, 2007). At local scales, however, fly visitation patterns often show strong species preferences, or even specificity (Bultman & Leuchtmann, 2003). Steinebrunner et al. showed that VOCs were important in the specific attraction of Botanophila flies to Epichloë stromata. Furthermore, using electroantennographic experiments and field bioassays (odour traps baited with pure synthetic compounds), they found that attraction resided in two unusual stromata-emitted compounds. One of these was the sesquiterpene alcohol chokol K, known only from Epichloë and already identified by the same group as a Botanophila attractant (Schiestl et al., 2006). The second, an unrelated compound identified in the current study as methyl (Z)-3-methyldodec-2-enoate, is a new natural product, also known only from Epichloë. A third compound, still unidentified, was not always present and elicited electrophysiological responses only from some individuals of one of the Botanophila taxa studied. The basis of olfactory attraction is therefore quite different from that in more generalized insect–fungal 'pollination' systems. The pseudoflowers of Puccinia rusts, for example, produce a complex blend of common floral volatiles (Raguso & Roy, 1998). By contrast, chemical communication in the Epichloë–Botanophila system is mediated by simple blends of a few compounds, as in a number of highly specific plant–insect pollination mutualisms, for example, those between figs and fig wasps (Grison-Pigéet al., 2002b), Yucca and Tegeticula moths (Svensson et al., 2006), and the dwarf palm and palm flower weevil (Dufaÿet al., 2004). In the Epichloë–Botanophila mutualism, as in some of these pollination mutualisms (e.g. the Yucca–Tegeticula system), the few compounds present are highly unusual substances. Specialization of chemically mediated communication in this insect–fungal 'pollination' system thus appears to have entailed reliance on a few system-specific molecules. Steinebrunner et al. call such signals 'private channels', a concept already used in previous studies of the evolution of signals in interspecies interactions (Schaefer et al., 2004). Steinebrunner et al. found no evidence of specificity of attraction at the species level. In some specialized pollination mutualisms, such as those between Ficus and their pollinating agaonid wasps (Grison-Pigéet al., 2002a), specificity is sometimes ensured by species-specific blends of individual compounds, each of which is shared by different species. By contrast, the most common Botanophila species studied by Steinebrunner et al. was caught at equal frequency in traps using odour blends of two Epichloë species with very different proportions of the two compounds. As the authors note, under a scenario of mutual benefits, specialization of Epichloë species to a single Botanophila taxon would be predicted; the absence of specificity in attraction is thus puzzling. However, their study was limited in its species coverage: only one fly species was abundant in their study sites, and odours of only three Epichloë species were tested. The generality of this result thus remains to be established. Furthermore, factors other than odour can ensure specificity of associations. Because Epichloë produce stromata on flowering tillers of their hosts, differences in flowering time of the hosts of different Epichloë species could lead to phenological barriers between them (Bultman & Leuchtmann, 2003). Habitat barriers could also be important. Even if flies are attracted to stromata, they may require other stimuli to oviposit. Specificity of fungus–fly associations could also be reinforced by fungal postzygotic isolation mechanisms. Fly larvae may suffer reduced fitness when their mothers effect interspecific spermatia transfer, so that associations could be specific despite imperfect specificity of attraction. Last, after mating, the stromata turn yellow by accumulating carotenoids: this opens the possibility that visual cues have evolved as signals of the stromata state. For the insect, it would allow them to avoid laying eggs on stromata that are too old or already occupied, whereas for the fungus it would avoid too heavy a load of larvae. More information is needed about the natural history and life cycles of Botanophila flies, and on the nature of mutualistic benefits, before conclusions can be drawn about the degree of specificity of associations, and on whether the limited specificity of attraction noted by Steinebrunner et al. is truly surprising. For example, how tightly is fly fitness related to active and efficient intraspecific fertilization? It would be intriguing if, as in fig–wasp pollination mutualisms (Jousselin & Kjellberg, 2001), the answer to this question turned out to vary among species as a result of complex co-evolutionary dynamics. Epichloë and Botanophila are but two links in an intricate web of interactions. Relationships between the fungus and its grass hosts are fascinatingly complex. How do Botanophila flies fit into this complexity? Some Epichloë species protect their host from insect and vertebrate herbivores by producing alkaloids (Schardl, 1996; Gonthier et al., 2008). Are these compounds present in stromata and do they have any effect on the flies? Do they play any role in specificity at the larval stage? Because stromata are produced on flowering tillers of the grass host, their production reduces host seed set, and some Epichloë spp. are partially or fully castrating parasites (Schardl, 1996; Gonthier et al., 2008). In these species, transmission is exclusively horizontal via meiotic spores arising from stromata and dispersed by wind among grass hosts. Other species combine sexual reproduction (= horizontal transmission) with asexual reproduction (and thus vertical transmission) by extending vegetative tissues in infected plants to infect seeds before their dispersal (Schardl, 1996). Yet other Epichloë species reproduce exclusively asexually, with exclusively vertical transmission (the so-called Neotyphodium species, Selosse & Schardl, 2007). Such phenomena are strongly reminiscent of conflicts between mutualists over reproduction in several horizontally transmitted plant–insect protection and pollination mutualisms (Anstett et al., 1997; Yu & Pierce, 1998). As in these systems, conflicts over reproduction appear to have led to a diversity of outcomes. As essential gamete vectors in fungal sexual reproduction, the flies should influence fungus–host interactions and, in turn, should be influenced by them. For example, the mutualistic, vertically transmitted Epichloë lineages are often sterile hybrids between sexual Epichloëspp. (Selosse & Schardl, 2007): to what extent did Botanophila flies, by allowing unspecific fertilization, contribute to the rise of hybrids that, constrained to vegetative reproduction and thus to noncastrating vertical transmission, turn out to be hybrid mutualists of the host plant? How do signals for 'pollinator' attraction fit into the complex evolutionary dynamics suggested by what we know of the comparative biology of these systems? One cannot escape the impression that interesting times indeed await those who dare to tackle the pairwise interactions between Epichloë and Botanophila in the context of the entire web of interactions among plants, herbivores, endophytes, 'pollinators', other fungivores and the abiotic environment. The study by Steinebrunner and colleagues offers a first exciting glimpse into some of the possibilities. References Anstett MC, Hossaert-McKey M, Kjellberg F. 1997. Figs and fig pollinators: evolutionary conflicts in a coevolved mutualism. Trends in Ecology and Evolution 12: 94– 99. Bultman TL, Leuchtmann A. 2003. A test of host specialization by insect vector as a mechanism for reproductive isolation among entomophilous fungal species. Oikos 103: 681– 687. Dufaÿ M, Hossaert-McKey M, Anstett MC. 2004. 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