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Floral Function: Eff Ects of Traits on Pollinators, Male and Female Pollination Success, and Female Fi Tness Across Three Species of Milkweeds ( Asclepias) 1

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Floral Function: Eff Ects of Traits on Pollinators, Male and Female Pollination Success, and Female Fi Tness Across Three Species of Milkweeds ( Asclepias) 1 RESEARCH ARTICLE AMERICAN JOURNAL OF BOTANY Floral function: eff ects of traits on pollinators, male and female pollination success, and female fi tness across three species of milkweeds ( Asclepias ) 1 R a ffi ca J. La Rosa 2,3,4 and Jeff rey K. Conner 2 PREMISE OF THE STUDY: Central questions in plant reproductive ecology are whether the functions of fl oral traits in hermaphrodites create confl ict between sexes that could slow evolution, and whether individual fl oral traits function in pollinator attraction, effi ciency, or both. We studied how fl oral traits aff ect pollinator visitation and effi ciency, and how they aff ect male and female function and female fi tness within and across three Asclepias species that diff er in fl oral morphology. METHODS: Using separate multiple regressions, we regressed pollen removal, deposition, and fruit number onto six fl oral traits. We also used path analyses integrating these variables with pollinator visitation data for two of the species to further explore fl oral function and its eff ects on fruit production. KEY RESULTS: Most traits aff ected male pollination success only, and these eff ects often diff ered between species. The exception was increased slit length, which increased pollinia insertion in two of the species. There were no interspecifi c diff erences in the eff ects of the traits on female pollination success. All traits except horn reach aff ected pollination effi ciency in at least one species, and horn reach and two hood dimensions were the only traits to aff ect pol- linator attraction, but in just one species. CONCLUSIONS: Traits tended to function in only one sex, and more traits aff ected function through pollinator effi ciency than through attraction. There was no signifi cant link between female pollination success and female fi tness in any of the three species; this pattern is consistent with fruit production not being limited by pollen deposition. KEY WORDS fl oral function; natural selection gradient; path analysis; plant-pollinator interactions Flowers of animal-pollinated plants function to manipulate polli- Most fl owering plants are hermaphroditic, so fl oral traits can nators into transporting pollen among fl owers. Floral traits attract function to increase pollen export (male function) and/or pollen pollinators (e.g., Mitchell, 1994 ; Conner and Rush, 1996 ; Schemske receipt (female function). Individual fl oral traits of hermaphroditic and Bradshaw, 1999 ; Johnson et al., 2003 ; Hansen et al., 2012 ), of- fl owers can act in harmony ( Delph and Ashman, 2006 ) by aff ecting ten reward them (e.g., Real and Rathcke, 1991 ; Silva and Dean, male and female function in the same direction (common adaptive 2000 ), and promote effi cient pollen transfer (e.g., Nilsson et al., peaks; Sahli and Conner, 2011 ) or by aff ecting only one sexual 1987 ; Fulton and Hodges, 1999 ; Conner et al., 2009 ). If increased function (specialization). Alternatively, traits may be in confl ict or pollination success results in increased fi tness, selection will act on experience tradeoff s by aff ecting male and female function in op- those fl oral traits that infl uence pollination. posing directions. Functional confl ict between the sexes can slow the evolution of a trait, but in most species studied to date, trait 1 Manuscript received 8 September 2016; revision accepted 19 December 2016. function is in harmony or is specialized ( Maad and Alexandersson, 2 W. K. Kellogg Biological Station, Department of Plant Biology, and Program in Ecology, 2004 ; Sahli and Conner, 2011 ; reviewed by Delph and Ashman, Evolutionary Biology and Behavior, Michigan State University, 3700 E. Gull Lake Dr., 2006 ). One way harmony can be achieved is through greater polli- Hickory Corners, Michigan 49060 nator visitation ( Delph and Ashman, 2006 ), which should increase 3 Current address: Department of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, CO 80309 female function until pollen is no longer limiting and increase male 4 Author for correspondence (e-mail: raffi [email protected] ) function until no more unfertilized ovules are available in the pop- doi:10.3732/ajb.1600328 ulation. However, in most studies that have examined trait eff ects 150 • AMERICAN JOURNAL OF BOTANY 104 (1): 150 – 160 , 2017; http://www.amjbot.org/ © 2017 Botanical Society of America JANUARY 2017 , VOLUME 104 • LA ROSA AND CONNER—MILKWEED FLORAL TRAIT FUNCTION • 151 on both male and female function, data on natural pollinator visita- et al., 2006 ; Maad, 2007 ). Milkweeds also have a history of provid- tion rates were not included (but see Galen and Stanton, 1989 ; ing insight into the eff ects of fl ower number on male and female Mitchell, 1994 ; Gómez et al., 2006 ; Campbell et al., 2014 ). function ( Willson and Rathcke, 1974 ; Willson and Price, 1977 ), but Hypotheses of fl oral function can be tested by collecting data on there are fewer examples of fl oral trait function. pollinator behavior to tease apart fl oral traits into those that act to To our knowledge, only two studies ( Morgan and Schoen, 1997 ; attract pollinators (e.g., fl oral color, Stanton et al., 1986 ; corolla Caruso et al., 2005 ) have measured phenotypic selection on fl oral size, Fenster et al., 2006 ; fl oral scent, Raguso, 2008 ), and those that morphology in A. syriaca , using the pollination measures of polli- function to eff ectively transfer pollen to and from the pollinator narium removal and pollinium insertion as estimates of male and (e.g., stigma and anther exertion, Conner et al., 1995 ; anther color female fi tness, respectively; however, neither study considered the and position, Ushimaru et al., 2007 ; spur length, Sletvold et al., specifi c functions of individual traits for pollinator attraction or ef- 2010 ). Studies integrating traits, measures of pollination and fi t- fi ciency. Our study integrates data on fl oral traits, pollinator visita- ness, and pollinator visitation allow us to identify these relation- tion, pollen removal and deposition, and female fi tness (fruits ships ( Gómez et al., 2006 ). Traits that act to attract pollinators have produced) in three locally co-occurring species of milkweeds with in some cases been shown to similarly aff ect both sexes ( Baranzelli divergent pollinators and fl oral traits. et al., 2014 ), and traits aff ecting the effi ciency (i.e., proportion of Th e three species in our study, the closely related Asclepias syri- successful pollination per visit) of pollinators, such as fl oral tube aca and A. tuberosa L. ( Fishbein et al., 2011 ), and A. viridifl ora Raf., length, can aff ect both sexes (e.g., Nilsson, 1988 ), or sometimes be share many of the same fl oral traits unique to milkweeds, but the specialized for one sex (e.g., Sahli and Conner, 2011 ; reviewed in fl owers of these species are diverse in size, shape, and color ( Fig. 2 ). Delph and Ashman, 2006 ). While they are oft en visited by honeybees, bumblebees, and wasps, Understanding how traits function in one species may enable the composition of pollinators diff ers between species, as shown in predictions about function in other species, especially with knowl- other studies ( Kephart, 1983 ; Betz et al., 1994 ; Fishbein and Venable, edge about trait distributions and selective agents in each species. 1996 ; Ivey et al., 2003 ; Stoepler et al., 2012 ). We measured six fl oral For example, predators may select similarly on insect wing dimen- traits that might interact with pollinators to aff ect pollination suc- sions or coloration ( Svensson and Friberg, 2007 ), or long tongued cess ( Fig. 2 ). All but one (gynostegium width) were measured in the nectar-feeders can select for convergence or divergence of fl oral two prior studies on A. syriaca ( Morgan and Schoen, 1997 ; Caruso tube or nectar spur length ( Johnson and Steiner, 1997 ; Manning et al., 2005 ). and Goldblatt, 1997 ; Whittall and Hodges, 2007 ). In this paper, we Our study addresses the following three questions: (1) Are there address fl oral function across sexes in three species of milkweeds. confl icts between male and female fl oral trait function? (2) Are Milkweeds ( Asclepias L.) are eudicots that have unusual her- there diff erences in function and selection on the same traits in maphroditic fl owers ( Fig. 1 ) and show convergence of fl oral struc- closely related species, and if there are diff erences, can they be ex- tures only with the distantly related orchid family (Orchidaceae). plained by selective agents and/or interspecifi c mean diff erences in Pollen grains are clustered into pollinia, which enable more precise the traits? (3) Do individual fl oral traits function more for attract- estimates of pollination success than is possible in most angio- ing pollinators or the effi ciency of pollen transfer? Seed production sperms with loose pollen. By scoring the number of pollinaria (at- of milkweeds is oft en resource limited ( Willson and Price, 1980 ; tached pairs of pollinia) removals and insertions, orchids and Caruso et al., 2005 ), which can reduce or eliminate the relationship milkweeds are ideal for studies of fl oral function through both between pollen deposition and female fi tness, weakening selection sexes. Orchids have been used to study the eff ects of traits and on fl oral traits that aff ect pollen deposition. By focusing our com- fl ower number on male and female function and female fi tness parison between sexes on pollination success, rather than seed set, (e.g., Nilsson, 1988 ; O’Connell and Johnston, 1998 ; Benitez-Vieyra we should be able to detect eff ects of traits on the pollination suc- cess of each sex to understand function. We predict that the traits that aff ect pollinator at- traction will infl uence male and female polli- nation success similarly, and that traits that aff ect pollination effi ciency will more oft en be specialized (aff ecting just one sex) or be in confl ict ( Delph and Ashman, 2006 ).
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