Winning in Style: Longer Styles Receive More Pollen, but Style Length Does Not Affect Pollen Attrition in Wild Clarkia Populations

RESEARCH ARTICLE A M E R I C A N J O U R N A L O F B O TA N Y I N V I T E D PA P E R For the Special Issue: Ecology and Evolution of Pollen Performance Winning in style: Longer styles receive more pollen, but style length does not aff ect pollen attrition in wild Clarkia populations 1 Susan J. Mazer 2 , Arrash Moghaddasi , Alexandra K. Bello 3 , and Alisa A. Hove PREMISE OF THE STUDY: One proposed function of long styles is to intensify selection among male gametophytes relative to short styles. If so, given suffi - cient competition, longer styles will have higher rates of pollen tube attrition (failure to reach the style base) within the style than shorter ones. Alterna- tively, style length may infl uence pollen receipt, which itself may aff ect attrition rates. METHODS : We tested these predictions by collecting senescing styles from wild populations of two insect-pollinated Clarkia species. We examined the number of pollen grains adhering to the stigma, length of styles, and rates of attrition from the stigma surface to the stigma–style junction (SSJ), from the SSJ to the style base, and from the stigma surface to the style base. Multivariate analyses estimated the independent eff ects of pollen grains per stigma, the number of pollen tubes at the SSJ, and style length on attrition. KEY RESULTS: Style length was generally positively correlated with pollen receipt, and the number of pollen grains per stigma was positively correlated with all three attrition rates. In neither species was any attrition rate aff ected by style length independent of the number of pollen grains per stigma. CONCLUSIONS: Pollen attrition was mediated by style length, but the function of style length was primarily to increase the number of germinating pollen grains, which aff ected attrition rates either through stigma clogging or pollen–pollen interactions. Style length may have a direct eff ect on pollen receipt due to the stigma’s position relative to pollinator body parts, but traits correlated with style length may also directly aff ect pollen receipt. KEY WORDS Clarkia unguiculata ; Clarkia xantiana subsp. xantiana ; gametophytic competition; Onagraceae; pollen attrition; pollen competition; pollen deposition; sexual selection; style length Diff erences in fl oral structure and morphology among taxa and be- tween genders have been interpreted as adaptations to alternative mating systems, pollination syndromes, and gender-specifi c repro- ductive costs, and as evolutionary responses to sexual selection on traits associated with increases in male fi tness ( Bell, 1985 ; Conner et al., 1996 ; Barrett, 2002 ; Barrett and Harder, 2005 ; Jacquemyn et al., 2005 ; Carlson and Harms, 2006 ; Ruan et al., 2011 ; Temeles et al., 2012 ; Barrett and Hough, 2013 ). Similar to many fl oral traits, style length exhibits notable phenotypic variation within natural popu- lations of many homomorphic plant species (i.e., excluding het- erostylous species), as well as among taxa ( Elmqvist et al., 1993 ; Manuscript received 1 May 2015; revision accepted 14 September 2015. Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, California 93105 USA Author for correspondence (e-mail: mazer@lifesci.ucsb.edu) Present address: Biology Department, Warren Wilson College, CPO 6217 PO Box 9000, Asheville, North Carolina 28815-9000 USA doi:10.3732/ajb.1500192 Ganeshaiah et al., 1999 ; Klinkhamer and van der Veen-van Wijk, 1999 ; Sarkissian and Harder, 2001 ; Travers and Shea, 2001 ; Bernasconi et al., 2007 ; Nattero and Cocucci, 2007 ; Kulbaba and Worley, 2008 ; Nattero et al., 2010 ; Forrest et al., 2011 ; Medrano et al., 2012 ; Jia and Tan, 2012 ; Wright et al., 2012 ). Th is variation has motivated a num- ber of experimental, observational, and comparative approaches to explain its ecological function and the evolutionary signifi cance of variation both within and among species. Experimental work has identifi ed reproductive and ecological functions of style length in several species ( Mulcahy and Mulcahy, 1975 ; Johnston, 1993 ; Forrest et al., 2011 ). Within-population sur- veys have examined phenotypic correlations between style length and other traits, such as functional gender, herkogamy, the number of pollen tubes within the style, pollen deposition by different pollinators, and corolla depth ( Mulcahy, 1979 ; Campbell, 1989 ; Klinkhamer and van der Veen-van Wijk, 1999 ; Bernasconi et al., 2007 ; Nattero and Cocucci, 2007 ; Forrest et al., 2011 ; Medrano et al., 2012 ). Comparisons between species that diff er in style length have A M E R I C A N J O U R N A L O F B OTA N Y 103 (3): 1 – 15 , 2016; http://www.amjbot.org/ © 2016 Botanical Society of America • 1