Down the Tube: Pollinators, Predators, and the Evolution of Flower Shape in the Alpine Skypilot, Polemonium Viscosum

Abstract

Abstract. We address how a conflict between pollinator attraction and avoidance of flower predation influences the evolution of flower shape in Polemonium viscosum. Flower shape in P. viscosum is the product of an isometric relationship between genetically correlated (r A ϭ 0.70) corolla flare and length. Bumblebee pollinators preferentially visit flowers that are more flared and have longer tubes, selecting for a funnel-shaped corolla. However, flower shape also influences nectar-foraging ants that sever the style at its point of attachment to the ovary. Surveys of ant damage show that plants having flowers with flared, short corollas are most vulnerable to ant predation. Consistent with this result, the ratio of corolla length to flare is significantly greater in a krummholz (high predation risk) population than in a tundra (low predation risk) population. To explicitly test whether the evolution of a better defended flower would exact a cost in pollination, we created tubular flowers by constricting the corolla during development. Performance of tubular flowers and natural controls was compared for defensive and attractive functions. In choice trials, ants entered control flowers significantly more often than tubular ones, confirming that the evolution of tubular flowers would reduce the risk of predation. However, in a bumblebee-pollinated population, tubular flowers received significantly less pollen and set fewer seeds than controls. A fitness model incorporating these data predicts that in the absence of the genetic correlation between corolla length and flare, intermittent selection for defense could allow tubular flowers to spread in the krummholz population. However, in the tundra, where bumblebees account for nearly all pollination, the model predicts that tubular flowers should always confer a fitness disadvantage.

Using theories of sexual selection and sexual conflict to improve our understanding of plant ecology and evolution

“…Floral traits that increase pollinator visits can also attract antagonistic insects and vectors for pathogens (Strauss and Whittall 2006; McArt et al 2014), and infection risk can differ between male and female plants (Shykoff et al 1996; Kaltz and Shykoff 2001). Thus, selection for, for example, large flowers can be affected by a compromise between sexual selection to attract pollinators and natural selection to avoid pathogens (Galen and Cuba 2001; Elzinga et al 2007; Burkhardt et al 2012), in either sexual function (see Box 1). Several traits connected with reproductive success are also indirectly negatively affected by herbivory and diseases, including flower morphology and pollinator visits (Strauss et al 1996), and pollen competitive ability (Stephenson et al 2003).…”

Herbivory as an important selective force in the evolution of floral traits and pollinator shifts

“…Many studies have examined floral adaptations to pollinators but we have only begun to appreciate the role of non-pollinator interactions in shaping plant reproductive biology (Strauss and Whittall 2006; Armbruster et al 2009; Johnson et al 2014). One such interaction, herbivory, can impose strong selection on floral colour (Irwin et al 2003; Frey 2004; Carlson and Holsinger, 2012), floral scent (Gross et al 2016), morphology (Galen and Cuba 2001; Sun et al 2016), flowering phenology (Brody 1997) and even mating systems (Kariyat et al 2013; Carr and Eubanks 2014), traits typically attributed to selection by pollinators. In a classic example, Galen and Cuba (2001) showed that both bumblebee pollinators and nectar-thieving ants preferentially visit flowers with larger floral flares in Polemonium viscosum (Polemoniaceae).…”

Differences in style length confer prezygotic isolation between two dioecious species ofSilenein sympatry

“…However, the selection on flower size (and hence style length) has been shown to be imposed by a variety of biotic and abiotic factors, including pollinators (Sandring and Ågren 2009; Parachnowitsch and Kessler 2010; Dudash et al. 2011), herbivores (Galen and Cuba 2001), and water availability (Galen 2000; Mojica and Kelly 2010). As a consequence, even though style length might differ in sympatry, reinforcement is only one possible underlying cause.…”