Phenotypic Selection Varies with Pollination Intensity Across Populations of Sabatia Angularis
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Research Phenotypic selection varies with pollination intensity across populations of Sabatia angularis Sarah L. Emel1, Steven J. Franks2 and Rachel B. Spigler1 1Department of Biology, Temple University, BioLife Building, 1900 N. 12th St, Philadelphia, PA 19122, USA; 2Department of Biological Sciences, Fordham University, Larkin Hall, 441 E. Fordham Road, Bronx, NY 20458, USA Summary Author for correspondence: Pollinators are considered primary selective agents acting on plant traits, and thus variation Rachel B. Spigler in the strength of the plant–pollinator interaction might drive variation in the opportunity for Tel: +1 215 204 8855 selection and selection intensity across plant populations. Here, we examine whether these Email: [email protected] critical evolutionary parameters covary with pollination intensity across wild populations of Received: 9 December 2016 the biennial Sabatia angularis. Accepted: 5 April 2017 We quantified pollination intensity in each of nine S. angularis populations as mean stig- matic pollen load per population. For female fitness and three components, fruit number, fruit New Phytologist (2017) set (proportion of flowers setting fruit) and number of seeds per fruit, we evaluated whether doi: 10.1111/nph.14608 the opportunity for selection varied with pollination intensity. We used phenotypic selection analyses to test for interactions between pollination intensity and selection gradients for five Key words: fitness components, flowering floral traits, including flowering phenology. phenology, flowering synchrony, opportunity The opportunity for selection via fruit set and seeds per fruit declined significantly with for selection, petal area, phenotypic increasing pollen receipt, as expected. We demonstrated significant directional selection on selection, plant–pollinator interactions, multiple traits across populations. We also found that selection intensity for all traits depended Sabatia angularis. on pollination intensity. Consistent with general theory about the relationship between biotic interaction strength and the intensity of selection, our study suggests that variation in pollination intensity drives variation in selection across S. angularis populations. populations (Benkman, 2013; Vanhoenacker et al., 2013). For Introduction mutualistic relationships such as plant–pollinator interactions, Understanding patterns of selection within and among natural decreased interaction strength is expected to result in reduced populations is a major goal in evolutionary biology. For plant mean absolute fitness of the population and, as a general conse- species that rely on pollinators for successful reproduction, quence, increased variance in relative fitness (Rundle & Vamosi, plant–pollinator interactions are predicted to play critical roles in 1996; Benkman, 2013; Vanhoenacker et al., 2013). It is this vari- shaping selection on traits related to pollen receipt and export ance in relative fitness that represents the opportunity for selec- (Harder & Barrett, 2006; Harder & Johnson, 2009). Indeed, tion (Crow, 1958; Arnold & Wade, 1984). Moreover, for traits experimental studies have demonstrated pollinator-mediated that influence fitness and are at the interface of the interaction, selection on a number of floral traits within populations (e.g. the strength of selection should also covary with biotic interaction Johnston, 1991; Caruso, 2000; Alexandersson & Johnson, 2002; strength (Benkman, 2013; Vanhoenacker et al., 2013), such that Sandring & Agren, 2009; Sletvold et al., 2010; Chapurlat et al., selection on floral traits should be greatest where plant–pollinator 2015; Lavi & Sapir, 2015). Given that pollinator and mate avail- interactions are weakest. Bartkowska & Johnston (2015) also ability are well known to be variable among populations, it fol- showed that this prediction arises from a simple arithmetic lows that selection on floral traits should covary with plant– relationship between selection intensity and one metric of plant– pollinator interaction strength among populations within species, pollinator interaction strength, pollen limitation (i.e. the relative yet few have evaluated this prediction (Vanhoenacker et al., increase in seed production from pollen-supplemented flowers or 2013; Sletvold & Agren, 2014; Bartkowska & Johnston, 2015). plants relative to controls; Larson & Barrett, 2000; Ashman et al., Specifically, both the opportunity for selection and selection 2004; Eckert et al., 2010). Others have considered the influence strength are predicted to increase with diminished plant–pollina- of plant–pollinator interactions on selection in terms of resource tor interactions. This expectation follows recent ecological theory availability, viewing pollen as a resource (Wilson, 1995; Rundle pointing more generally to spatial variation in biotic interaction & Vamosi, 1996), with the analogous prediction that, as pollen strength as key to explaining variation in selection across loads decline, selection on traits related to pollen import and Ó 2017 The Authors New Phytologist (2017) 1 New Phytologist Ó 2017 New Phytologist Trust www.newphytologist.com New 2 Research Phytologist export should increase (Rundle & Vamosi, 1996). This expecta- Materials and Methods tion should hold even if some pollen deposition is attributable to autonomous self-pollination. Therefore, here we use the more Study system general term ‘pollination intensity’. Importantly, these predic- tions may be met only where variation in pollination intensity is Sabatia angularis (L.) Pursh (Gentianaceae) is native to the east- relevant, that is, where seed production can be improved by ern USA and Canada. Widely distributed throughout its range, it increased pollination (Campbell & Halama, 1993; Campbell & is found in a diversity of habitats including marshes, dry prairies Bischoff, 2013; Vanhoenacker et al., 2013). Otherwise, beyond and glades, roadsides, and serpentine barrens. A biennial, its seeds some point, seed production and thus selection resulting from disperse in the fall, germinate in the spring and form rosettes that plant–pollinator interactions saturate with continuing increases overwinter until the following spring, when plants bolt. From in pollen receipt. July to August, the plants produce displays of showy pink, Previous studies provide insight into the traits most likely to protandrous flowers, which develop into many-seeded dry dehis- be selected for by pollinators and thus result in more reliable cent capsules. The self-compatible flowers are nectarless but do pollination (Knight et al., 2005). Pollinators are expected to have a scent and offer a pollen reward to a suite of generalist floral favor plants with traits that promote attraction, ranging from visitors including leaf-cutter bees (Megachilidae), sweat bees greater flower number, size, and floral display to color or (Halictidae), andrenid bees (Andrenidae), bumblebees (Apidae), greater overall plant size (Harder & Barrett, 2006; Harder & small carpenter bees (Anthophoridae), and hover flies (Syrphidae) Johnson, 2009; Campbell & Bischoff, 2013). Rarer are studies (Dudash, 1987; Spigler, 2007). of selection on floral phenological traits, but these traits may Prior work has demonstrated that pollen receipt varies widely also be under selection by pollinators (reviewed in Munguıa- among populations of S. angularis (Spigler & Chang, 2008) and Rosas et al., 2011). Of the few studies investigating selection that both fruit and seed production can be pollen limited on phenological traits, most have focused on date of first or (Dudash, 1993; Spigler & Chang, 2009). Much higher pollen last flower (e.g. Sandring & Agren, 2009; Sletvold & Agren, limitation occurs for seeds per fruit, given that a single fruit can 2014; Chapurlat et al., 2015; and see Munguıa-Rosas et al., produce anywhere between several and > 1000 seeds (Dudash, 2011). Other phenological traits such as flowering duration 1993; Spigler & Chang, 2008). Moreover, flower number per and synchrony may also be important. For example, pollinators plant varies markedly in this monocarpic species, with plants pro- might be more likely to visit plants that flower synchronously ducing anywhere from a single flower to upwards of 300. Thus, with the rest of the population (e.g. Augspurger, 1981; Rathke flower number not only probably influences pollinator attraction & Lacey, 1985), or alternatively, asynchronous flowering may via floral display, but also sets an upper limit on fruit number be favored where competition for pollinators is high (Elzinga and consequently female fitness. Together, fruit number and et al., 2007). Selection on these traits should be greatest where number of seeds per fruit are expected to lead to wide variation pollination intensity is lowest. in fitness among plants, particularly where pollen loads are low. Support for the hypotheses that the opportunity for selection Populations of S. angularis vary greatly in size (Spigler & Chang, and selection strength covary with pollination intensity thus far 2008), but importantly pollen limitation can occur in both small has been equivocal. The few studies evaluating the strength of and large populations (Dudash, 1993; Spigler & Chang, 2009; selection on a number of floral traits in relation to pollen limita- R. B. Spigler, unpublished) and pollen loads need not correlate tion across species provide general support (Ashman & Morgan, with population size or density (Spigler & Chang, 2008). Popu- 2004; Sletvold & Agren, 2014; Bartkowska & Johnston,