Abstract

Nectarless flowers that deceive pollinators offer an opportunity to study asymmetric plant-insect interactions. Orchids are a widely used model for studying these interactions because they encompass several thousand species adopting deceptive pollination systems. High levels of intra-specific phenotypic variation have been reported in deceptive orchids, suggesting a reduced consistency of pollinator-mediated selection on their floral traits. Nevertheless, several studies report on widespread directional selection mediated by pollinators even in these deceptive orchids. In this study we test the hypothesis that the observed selection can fluctuate across years in strength and direction thus likely contributing to the phenotypic variability of this orchid group. We performed a three-year study estimating selection differentials and selection gradients for nine phenotypic traits involved in insect attraction in two Mediterranean orchid species, namely Orchis mascula and O. pauciflora, both relying on a well-described food-deceptive pollination strategy. We found weak directional selection and marginally significant selection gradients in the two investigated species with significant intra-specific differences in selection differentials across years. Our data do not link this variation with a specific environmental cause, but our results suggest that pollinator-mediated selection in food-deceptive orchids can change in strength and in direction over time. In perennial plants, such as orchids, different selection differentials in the same populations in different flowering seasons can contribute to the maintenance of phenotypic variation often reported in deceptive orchids.

Highlights

  • Pollinator-mediated selection is one of the main processes driving the evolution of floral traits in entomophilous pollen-limited plant species (Fenster et al, 2004)

  • Pollination success was found to be correlated with plant height in Cypripedium acaule (O’Connell & Johnston, 1998), to the number of flowers in Anacamptis morio (Johnson & Nilsson, 1999), to spur length in the Disa draconis species complex (Johnson & Steiner, 1997) and in hybrid zones between Anacamptis morio and A. longicornu (Zitari et al, 2012), to flowering time in some deceptive orchids (Sabat & Ackerman, 1996; O’Connell & Johnston, 1998; Sun et al, 2009; but see Sletvold, Grindeland & Ågren, 2010), to plant height, flower number and spur length in Dactylorhiza lapponica (Sletvold, Grindeland & Ågren, 2010) and to flower brightness and contrast in Anacamptis morio (Sletvold et al, 2016). This evidence is unexpected, considering the high levels of phenotypic variation seen in deceptive orchids and suggests that, even in this plant group, directional selection mediated by pollinators may be widespread and strong

  • The quantification and interpretation of the direction, strength and causes of natural selection have been at the centre of scientific debate since the formulation of Darwin’s theory (Darwin, 1859)

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Summary

INTRODUCTION

Pollinator-mediated selection is one of the main processes driving the evolution of floral traits in entomophilous pollen-limited plant species (Fenster et al, 2004). Pollination success was found to be correlated with plant height in Cypripedium acaule (O’Connell & Johnston, 1998), to the number of flowers in Anacamptis morio (Johnson & Nilsson, 1999), to spur length in the Disa draconis species complex (Johnson & Steiner, 1997) and in hybrid zones between Anacamptis morio and A. longicornu (Zitari et al, 2012), to flowering time in some deceptive orchids (Sabat & Ackerman, 1996; O’Connell & Johnston, 1998; Sun et al, 2009; but see Sletvold, Grindeland & Ågren, 2010), to plant height, flower number and spur length in Dactylorhiza lapponica (Sletvold, Grindeland & Ågren, 2010) and to flower brightness and contrast in Anacamptis morio (Sletvold et al, 2016) This evidence is unexpected, considering the high levels of phenotypic variation seen in deceptive orchids and suggests that, even in this plant group, directional selection mediated by pollinators may be widespread and strong (but see Cintrón Berdecía & Tremblay, 2003). We used two orchid species with similar flower morphology and a common set of pollinators (Van Der Cingel, 1995; Cozzolino et al, 2006; Nilsson, 2008; Valterovà et al, 2007) as replicates to increase the power of our conclusions for Mediterranean food-deceptive orchids

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