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Mating Opportunity Increases with Synchrony of Flowering Among Years More Than Synchrony Within Years in a Nonmasting Perennial

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Mating Opportunity Increases with Synchrony of Flowering Among Years More Than Synchrony Within Years in a Nonmasting Perennial vol. 192, no. 3 the american naturalist september 2018 Mating Opportunity Increases with Synchrony of Flowering among Years More than Synchrony within Years in a Nonmasting Perennial Amy Waananen,1,2,* Gretel Kiefer,3 Jennifer L. Ison,4 and Stuart Wagenius1 1. Division of Plant Science and Conservation, Chicago Botanic Garden, Glencoe, Illinois 60022; 2. Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, Minnesota 55108; 3. The Echinacea Project, Kensington, Minnesota 56343; 4. Department of Biology, College of Wooster, Wooster, Ohio 44691 Submitted May 17, 2017; Accepted April 6, 2018; Electronically published June 18, 2018 Online enhancements: appendixes. Dryad data: http://dx.doi.org/10.5061/dryad.487db24. abstract: 2007; Munguía-Rosas et al. 2011). Likewise, among-year The timing and synchrony of mating activity in a popu- fi lation may vary both within and among years. With the exception of timing of mating can be de ned as the year or years that in- masting species, in which reproductive activity fluctuates dramatically dividuals exert reproductive effort. For many iteroparous among years, mating synchrony is typically studied within years. species, reproductive years may be interspersed with years However, opportunities to mate also vary among years in nonmasting of reproductive inactivity (Kelly and Sork 2002). Because iteroparous species. We demonstrate that studying only within-year plants are immobile and cannot compensate for spatial iso- fl owering synchrony fails to accurately quantify variation in mating lation from potential mates by active searching, timing of opportunity in an experimental population (n p 286) of a nonmast- ing species, Echinacea angustifolia. We quantified individuals’ syn- mating is especially critical to their mating success. The chrony of flowering within and among years and partitioned the con- consequences of synchronizing mating among years have tribution of each measure to mean daily mating potential, the number received considerable attention in masting species (i.e., of potential mates per individual per day, averaged over every day that those that reproduce with a high degree of variation among it flowered during the 11-year study period. Individual within- and years; Taylor and Inouye 1985; de Steven and Wright 2002; among-year synchrony displayed wide variation and were weakly cor- Wesołowski et al. 2015). In contrast, the consequences of related. In particular, among-year synchrony explained 39% more synchronizing mating among years are rarely considered variation in mean daily mating potential than did within-year syn- fi in nonmasting species. chrony. Among-year synchrony could have underappreciated signi - fi fi cance for mating dynamics in nonmasting species. De nitions of mating synchrony are speci c to a level of organization (i.e., population or individual) and a tempo- Keywords: phenology, masting, reproductive fitness, mate limitation, ral scale (i.e., within or among years). At the population Echinacea angustifolia. level, variation in the number of individuals seeking to mate simultaneously, either within or among years, can be fi fi Introduction quanti ed as population synchrony ( g. 1; Koenig et al. 1994; Crone et al. 2009; Archibald et al. 2012; Kaiser et al. The time when individuals are available to mate deter- 2017). Similarly, we measure individual synchrony as how mines the number and identity of their potential partners an individual’s timing of mating aligns with the mating (Calabrese and Fagan 2004; Hendry and Day 2005; Elzinga activity of the population within or among years. While re- et al. 2007; Gascoigne et al. 2009). Within-year timing, or productive synchrony could refer to other processes (e.g., phenology, of mating is defined by the days that an individ- sexual maturation, embryo development, or birth), we fo- ual is available to participate in mating activity (Forrest and cus on the synchrony of when individuals are available to Miller-Rushing 2010) and has important consequences for outcross or mate with other individuals. Outcrossing is reproductive success and selection (Ims 1990; Elzinga et al. obligatory for successful reproduction in most animals and self-incompatible plants, which comprise 60% of all plant * Corresponding author; email: [email protected]. ORCIDs: Waananen, http://orcid.org/0000-0002-7940-3210. species (de Nettancourt 2013). Opportunities for an indi- – q vidual to interact with prospective mates at either temporal Am. Nat. 2018. Vol. 192, pp. 379 388. 2018 by The University of Chicago. fi 0003-0147/2018/19203-57724$15.00. All rights reserved. scale can be quanti ed as mating potential: the number of DOI: 10.1086/698657 conspecifics available to mate with the individual. The mag- 380 The American Naturalist 180 a 2010 b 2011 c 2012 0.06 160 140 120 100 0.06 80 0.02 flowering plants flowering 60 40 0.03 0.07 20 0.03 0 −20 −10 0 10 20 −20 −10 0 10 20 −20 −10 0 10 20 days from peak Figure 1: Temporal distribution of mating potential in 2010–2012 (a–c, respectively), chosen to highlight within- and among-year variation in flowering in our study population. The X-axis indicates days after peak (the day with maximum number of individuals flowering) in each year, and the Y-axis indicates the number of individuals flowering. Lines indicate mating potential for each day. Dark and light shaded areas illustrate cumulative mating potential of hypothetical early- and peak-flowering individuals with each flowering 7 days. The total sum of potential mating interactions in 2010, 2011, and 2012 was 1,425, 3,062, and 585, respectively. The differences in absolute mating potential per year influence individuals’ among-year synchrony. Open circles are positioned at an individual’s mean within-year mating potential and are labeled with the individuals’ within-year synchrony (e.g., on average, 39 individuals were flowering on the same days as the early- flowering individual in 2010 [a], so its mean within-year mating potential in 2010 equals 39 and its within-year synchrony equals 39 divided by 1,425, or 0.03). nitude of fluctuations in population synchrony within and lived herbaceous perennial plant. We applied a novel statis- among years determines the importance of individual syn- tical approach to an 11-year data set of individual flowering chrony for individuals’ opportunities to outcross. For ex- phenology in a population of the narrow-leaved purple ample, consider two individuals that each reproduce in two coneflower (Echinacea angustifolia, Asteraceae; hereafter out of five years. One individual seeks to mate in the pop- “Echinacea”). Populations of this species vary in flowering ulation’s two peak years of mating activity, but late relative rates among years (Ison et al. 2014), but it is not considered to the peak activity within each year. The other individual to be masting. We (1) measured the degree of within- and seeks to mate in two off-peak years but at peak days of mat- among-year synchrony of the population and tested for de- ing activity for the population within each year. The differ- partures from expected flowering patterns using randomi- ence in mating potential between these two hypothetical in- zation techniques, (2) developed measures of individual syn- dividuals depends on the degree of population synchrony chrony that enabled us to partition the relative contribution both within and among years. Quantifying the relationship of within- and among-year synchrony to individuals’ long- between mating potential and synchrony both within and term mating potential using regression analysis, and (3) quan- among years would indicate the potential for timing at each tified how variation in the duration of mating activity among temporal scale to affect reproductive success (Inouye 2008; individuals influences mating potential. Forrest and Miller-Rushing 2010), mating patterns (Weis and Kossler 2004), and evolution of reproductive timing by nat- Methods ural selection (Devaux and Lande 2010). Study System and Field Monitoring In this study, we quantified the relative contributions of individual synchrony in flowering within and among years Our study focuses on a cohort of Echinacea plants in an to the long-term mating potential of individuals for a long- experimental plot located in Solem Township, Minnesota. Scales of Synchrony 381 These plants were collected as seeds from seven nearby nat- chrony may not necessarily predict reproductive success ural populations and then planted in 1996. We included all (seed set). For this reason, we limited analysis to measures plants that survived through 2015 and flowered at least of mating potential rather than reproductive success. Sim- once during 2005–2015, n p 286 individuals. A full de- ilarly, we did not analyze potential contributions of spatial scription of experiments in the plot can be found elsewhere isolation for predicting mating potential because the study (Geyer et al. 2007). Echinacea is a long-lived (125 year) pe- cohort is centrally located within the plot and appropriate rennial. Adult individuals may or may not flower in a given measures of spatial isolation would require considering year. In flowering years, individuals produce one or more proximity to neighbors outside of the cohort. We com- flowering heads, each comprising many florets (typically pleted all data analysis using R, version 3.2.4 (R Develop- 80–250). Multiple-headed individuals may flower longer ment Core Team 2016). to the extent that their heads do not flower concurrently. In nonflowering years, individuals produce one to several Population Synchrony rosettes of basal leaves. Echinacea is self-incompatible and bee-pollinated: reproduction in natural populations in our To quantify within-year population synchrony, we calcu- study site is mate-limited (Wagenius 2006; Wagenius and lated mean overlap in flowering of all pairs of individuals. Lyon 2010). The plot was burned regularly (in spring of We defined overlap for a pair as the number of days that 2006, 2008, 2011, 2013, and 2015).
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