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Evidence for Pollinator-Mediated Divergent Selection

To test for signatures of pollinator-mediated selection among three sympatric Ophrys species, Mant et al. (2005b) compared patterns of species divergence across active and nonactive volatiles, and neutral microsatellite genetic markers. Only the traits predicted to be under selection, the bioactive alkanes/alkenes, were strongly divergent. Xu et al. (2012) later reported the outcomes of additive bioassays. These showed that (Z)-7 alkenes strongly inhibited the attraction of the pollinator of

O. sphegodes (which uses a (Z)-9 alkene as pollinator attractant). Conversely, (Z)-9 alkenes inhibited the pollinator of O. exaltata (which uses a (Z)-7 alkene as pollinator attractant). Thus, strong pollinator-mediated divergent selection for alkene double-bond position is highly likely between these species.

Choice tests with Chiloglottis orchid pollinators also support the hypothesis of pollinator-mediated selection (Peakall et al. 2010). For example, the pollinator of C. valida, responded very strongly to chiloglottone 1 (93%), not at all to chiloglottone 3, and rarely (7%) to a 1:1 blend (Figure 15.4a). Conversely, the pollinator of C. aff. jeanesii, only responded to chiloglottone 3 (Figure 15.4b). The pollinator of C. chlorantha, responded strongly to chiloglottone 3 (71%), not at all to chiloglottone 1, and partially (29%) to a 1:1 blend (Figure 15.4c). Thus, strong pollinator-driven selection for floral chemistry matching the sex pheromone of the wasp is highly likely. One theory is that blends arising from initially neutral mutations might provide a bridge for pollinator-driven selection to drive chemical shifts and potentially speciation (Peakall et al., 2010, Peakall and Whitehead, 2014).

The Strength of Floral Isolation

The strength of reproductive isolation (RI) barriers between two species can be estimated quantitatively as an RI index (range negative to 1), where a value of 1 indicates complete isolation. Across plants generally, relatively few studies have quantified RI indices across a full range of pre- and postzygotic reproductive isolating barriers (Martin and Willis, 2007, Lowry et al., 2008). Among sexually deceptive orchids, two parallel studies in European Ophrys (Xu et al., 2011) and Australian Chiloglottis (Whitehead and Peakall, 2014) have comprehensively quantified the strength of pollinator, post-mating prezygotic and postzygote isolation as well as genetically assessed the natural rate of hybridization. Both studies found pollinator RI values >0.98, while postzygote RI values were zero or negative. Furthermore, very limited evidence for hybrids was found in the Ophrys case (2 out of 146 genetic samples), and no evidence for hybridization in the Chiloglottis case (0 out of 571 genetic samples). Hence, both cases stand out as extreme examples of the pre-eminence of pollinator isolation (Xu et al., 2011, Whitehead and Peakall, 2014). Furthermore, given that the pollinator specificity that maintains species boundaries is controlled by chemistry in these species, genic speciation (sensu Wu, 2001) via speciation genes associated with floral volatiles seems highly plausible.

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