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The Mechanism of Pollinator Specificity Between Two Sympatric Annals of Botany 111: 173–181, 2013 doi:10.1093/aob/mcs250, available online at www.aob.oxfordjournals.org The mechanism of pollinator specificity between two sympatric fig varieties: a combination of olfactory signals and contact cues Gang Wang1,2, Stephen G. Compton3 and Jin Chen1,* 1Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303, China, 2University of Chinese Academy of Science, Beijing 100039, China and 3School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, West Yorkshire LS2 9JT, UK * For correspondence. E-mail [email protected] Downloaded from https://academic.oup.com/aob/article/111/2/173/254661 by guest on 30 September 2021 Received: 4 April 2012 Returned for revision: 9 August 2012 Accepted: 11 October 2012 Published electronically: 23 November 2012 † Background and Aims Pollinator specificity facilitates reproductive isolation among plants, and mechanisms that generate specificity influence species boundaries. Long-range volatile attractants, in combination with mor- phological co-adaptations, are generally regarded as being responsible for maintaining extreme host specificity among the fig wasps that pollinate fig trees, but increasing evidence for breakdowns in specificity is accumulat- ing. The basis of host specificity was examined among two host-specific Ceratosolen fig wasps that pollinate two sympatric varieties of Ficus semicordata, together with the consequences for the plants when pollinators entered the alternative host variety. † Methods The compositions of floral scents from receptive figs of the two varieties and responses of their polli- nators to these volatiles were compared. The behaviour of the wasps once on the surface of the figs was also recorded, together with the reproductive success of figs entered by the two Ceratosolen species. † Key Results The receptive-phase floral scents of the two varieties had different chemical compositions, but only one Ceratosolen species displayed a preference between them in Y-tube trials. Specificity was reinforced at a later stage, once pollinators were walking on the figs, because both species preferred to enter figs of their normal hosts. Both pollinators could enter figs of both varieties and pollinate them, but figs with extra-varietal pollen were more likely to abort and contained fewer seeds. Hybrid seeds germinated at normal rates. † Conclusions Contact cues on the surface of figs have been largely ignored in previous studies of fig wasp host preferences, but together with floral scents they maintain host specificity among the pollinators of sympatric F. semicordata varieties. When pollinators enter atypical hosts, post-zygotic factors reduce but do not prevent the production of hybrid offspring, suggesting there may be gene flow between these varieties. Key words: Contact cues, Ficus semicordata, floral scents, host recognition, hybridization, pollination, pollinator specificity, reproductive isolation. INTRODUCTION number of species of pollinators, and thus contribute to the plants’ reproductive isolation. In the fig–fig wasp mutualism, Adaptations that favour pollination by a limited range of the volatile blends released from the figs of .40 Ficus species animal vectors have been a key factor in the diversification have been investigated (Ware et al., 1993; Grison et al., 1999; of flowering plants, with some of the most species-rich plant Song et al., 2001; Grison-Pige et al., 2002; Chen et al., 2009; groups characterized by extreme pollinator specificity Proffit et al., 2009; Soler et al., 2011), and their role in attracting (Darwin, 1876; Johnson, 2006; Raguso, 2008). Pollinator spe- their specific pollinators has been demonstrated in field trapping cificity is a pre-zygotic isolating mechanism that often deter- (Bronstein, 1987; van Noort et al., 1989; Ware and Compton, mines the extent of gene flow among taxa and consequently 1994b) and laboratory tests (Grison-Pige et al., 2002; Chen determines their species boundaries (Grant, 1994; Sargent, and Song, 2008; Chen et al., 2009; Proffit et al., 2009). It is 2004; Waser and Ollerton, 2006). Plants with plant-specific believed that species specificity in the fig–fig wasp system is pollinators often also display weak post-zygotic isolating generally mediated by species-specific volatile signals (van mechanisms, as in some Orchidaceae species (Schiestl and Noort et al., 1989; Chen et al., 2009; Hossaert-McKey et al., Schluter, 2009) and those genera associated with obligate 2010). Pollinator specificity that is driven primarily by plant nursery pollination mutualisms, such as Ficus (Ramirez, volatiles is also found in some other systems. Euglossine bee- 1970; Hossaert-McKey et al., 2010), Yucca (Pellmyr, 2003) pollinated neotropical orchids, and sexually deceptive orchids and Glochidion (Kato et al., 2003). Consequently, traits re- in Australia and Europe are examples (Ayasse et al., 2003; sponsible for maintaining pollinator specificity in these plant Schiestl et al., 2003; Eltz et al., 2005). Similarly, the groups with highly specific pollinators influence both repro- host-specific Epicephala moths that pollinate Breynia ductive isolation and the generation of novel diversity. vitis-idaea (Euphorbiaceae) have been shown to be attracted Specific floral scents are known to be a key element in pollin- by floral scent using both behavioural and electrophysiological ator attraction for many plants that have just one or a small methods (Svensson et al., 2010). # The Author 2012. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 174 Wang et al. — Mechanism of pollinator specificity in Ficus The one pollinator–one host Ficus relationship is not uni- Pollinator responses to volatiles have generally been moni- versal, and there are several reports of Ficus species with mul- tored using insects walking in Y-tube olfactometers, though tiple pollinator species (Rasplus, 1996; Kerdelhue et al., 1999; the responses of flying insects in the field have also been Molbo et al., 2003; Compton et al., 2009), or one pollinator tested (Bronstein, 1987; van Noort et al., 1989; Ware and species may be associated with more than one host taxon Compton, 1994b; Chen and Song, 2008; Chen et al., 2009; (Cornille et al., 2012). Those reports suggest that a relatively Proffit et al., 2009). Those studies have consistently detected loose form of coevolution has been occurring, at least in pollinator attraction to species-specific and developmental some lineages. Entry of pollinators into the figs of atypical stage-specific floral scents emanating from figs. However, at- Ficus hosts often results in fertile seeds, even among sympatric traction of fig wasps to their normal host does not necessarily Ficus species that are clearly distinct in terms of their ecology equate with the maintenance of absolute pollinator specificity, and morphology. This shows that post-zygotic barriers to hy- because infrequent arrivals at non-host figs have been recorded bridization are often weak in this genus (Ramirez, 1970; under field conditions, as has the entry of pollinators into figs Downloaded from https://academic.oup.com/aob/article/111/2/173/254661 by guest on 30 September 2021 Janzen, 1979; Parrish et al., 2003; Kusumi et al., 2012). of atypical host species (Bronstein, 1987; Ware and Compton, Therefore, the strength of pollinator specificity of each fig 1994b; Moe et al., 2011). In addition to these ‘mistakes’ where wasp largely determines species boundaries of figs (Machado long-range cues have been by-passed, some fig wasps may also et al., 2005). Factors among Ficus species that are likely to in- be attracted to figs of species other than their typical hosts, as crease the likelihood of figs being visited by the ‘wrong’ fig with the pollinator of F. microcarpa, which is attracted to figs wasps include living in sympatry, co-flowering phenologies, of F. fulva as well as to those of its normal pollinator similarities in fig size and shared compounds in the floral (Grison-Pige et al., 2002). Furthermore, for those closely scents released from their receptive figs (Whitehead and related fig species that are living in sympatry, behavioural Peakall, 2009; Hossaert-McKey et al., 2010). The extent to tests of fig wasp responses to floral scent cues could supply which phylogeny determines the components of floral scents more powerful evidence to understand the mechanism of pol- among Ficus species is unclear (Hossaert-McKey et al., linator specificity. 2010), but if closely related taxa produce more similar volatile Here, we use two sympatric varieties of an Asian fig tree, blends, then pollinator ‘mistakes’ that result in genetic ex- Ficus semicordata, that are host to two different pollinators, change may be more likely to occur among sister taxa. to investigate mechanisms of pollinator specificity among Sympatric or sister taxa can provide powerful insights into sympatric closely related fig taxa. Both volatile and short- floral scent-mediated reproductive isolation (Whitehead and range contact cues were investigated and the following specific Peakall, 2009). Ideal systems for studying the consequences questions were addressed. (1) Are the floral scents emitted by of floral fragrance variation should control for other confound- receptive-phase figs of the two varieties distinct? (2) Do floral ing abiotic and biotic variables, such as geographical and tem- scents alone maintain pollinator specificity or are contact cues
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