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A Mosaic of Phenotypic Variation in Giant Ragweed (Ambrosia Trifida): Local-­ and Continental-­Scale Patterns in a Range-­ Expanding Agricultural Weed

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A Mosaic of Phenotypic Variation in Giant Ragweed (Ambrosia Trifida): Local-­ and Continental-­Scale Patterns in a Range-­ Expanding Agricultural Weed Received: 13 November 2017 | Accepted: 3 February 2018 DOI: 10.1111/eva.12614 ORIGINAL ARTICLE A mosaic of phenotypic variation in giant ragweed (Ambrosia trifida): Local- and continental- scale patterns in a range- expanding agricultural weed Stephen M. Hovick1 | Andrea McArdle1 | S. Kent Harrison2 | Emilie E. Regnier2 1Department of Evolution, Ecology and Organismal Biology, The Ohio State Abstract University, Columbus, OH, USA Spatial patterns of trait variation across a species’ range have implications for popula- 2 Department of Horticulture and Crop tion success and evolutionary change potential, particularly in range- expanding and Science, The Ohio State University, Columbus, OH, USA weedy species that encounter distinct selective pressures at large and small spatial scales simultaneously. We investigated intraspecific trait variation in a common gar- Correspondence Stephen M. Hovick, Department of den experiment with giant ragweed (Ambrosia trifida), a highly variable agricultural Evolution, Ecology and Organismal Biology, weed with an expanding geographic range and broad ecological amplitude. Our study The Ohio State University, Columbus, OH, USA. included paired populations from agricultural and natural riparian habitats in each of Email: [email protected] seven regions ranging east to west from the core of the species’ distribution in cen- Funding information tral Ohio to southeastern Minnesota, which is nearer the current invasion front. We Ohio Agricultural Research and observed trait variation across both large-­ and small- scale putative selective gradi- Development Center, Ohio State University, Grant/Award Number: 2011-078; Division ents. At large scales, giant ragweed populations from the westernmost locations of Environmental Biology, Grant/Award were nearly four times more fecund and had a nearly 50% increase in reproductive Number: DEB-1146203; Cooperative State Research, Education, and Extension Service, allocation compared to populations from the core. The degree of surface texture on Grant/Award Number: GRANT11073659 fruits also declined from east to west. Greater fecundity in the west represents a putative trade- off between fruit size and fruit number across the study region, al- though no such trade- off was found across individual plants. This pattern may ef- fectively result in greater propagule pressure closer to the invasion front. At smaller spatial scales, plants from agricultural populations emerged later and were smaller than plants from riparian populations. However, because plants from agricultural populations allocated more biomass to reproduction, total fecundity did not differ across habitats. Our emergence data are consistent with previous observations showing delayed emergence in agricultural compared to natural populations; thus evolutionary change may be predictable as giant ragweed continues spreading into agricultural fields throughout North America. These shifts in life- history strategy ap- parently bear no fecundity cost, suggesting that giant ragweed’s success can be at- tributed at least in part to its substantial adaptive potential. KEYWORDS Ambrosia trifida, emergence timing, functional traits, intraspecific variation, local adaptation, seed size–seed number trade-off, seed surface texture, seedling emergence This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd Evolutionary Applications. 2018;1–15. wileyonlinelibrary.com/journal/eva | 1 2 | HOVICK ET AL. 1 | INTRODUCTION process underlying observed phenotypic variation, local adaptation will be much less likely because plasticity can effectively buffer pop- Intraspecific trait variation is common in many species, reflecting pro- ulations against local selective pressures (De Jong, 2005). In this cesses such as local adaptation, phenotypic plasticity, and variable case, similar genotypes may achieve highly divergent phenotypes gene flow across the landscape (Albert, Grassein, Schurr, Vieilledent, under variable abiotic or biotic conditions (Parker, Rodriguez, & Loik, & Violle, 2011). Particularly for species with large geographic distri- 2003). butions and ecological amplitudes, these processes may yield com- Although substantial research effort has gone into identifying plex, non- neutral spatial patterns of intraspecific variation (Bhattarai which traits should be most important for success among weedy and et al., 2017; Nelson & Anderson, 2015). A large geographic range invasive species (Pyšek & Richardson, 2008; Van Kleunen, Weber, & enhances the breadth of bioclimatic variation a species encoun- Fischer, 2010), much less emphasis has been given to within- species ters, and selection in response to such spatially continuous varia- variation (Albert et al., 2011), particularly across clinal gradients, dis- tion should result in trait autocorrelation among nearby populations tinct habitat types, or establishment centers versus invasion fronts. (Murray, Brown, & Grace, 2003). On the other hand, large ecological As a result, we may underestimate the importance of trait plasticity amplitudes that allow a species to occupy distinct habitats may lead and/or rapid evolutionary change in the colonization success of to local adaptation at small spatial scales (Hereford, 2009; Kittelson widespread weedy or invasive species (Whitney & Gabler, 2008; & Maron, 2001). Where distinct habitats occur repeatedly across a Williams, Kendall, & Levine, 2016). Assuming single trait values to species’ range, adaptation at large and small scales may occur simul- be static representations of a species with the ability to colonize a taneously, yielding a pattern of continuous variation overlain by re- wide range of site conditions also leads to an under- appreciation peated occurrences of local adaptation. Whether and how a species of intraspecific trade- offs among traits. For example, fecundity is partitions its phenotypic variation across such complex landscapes a commonly cited predictor of invasiveness in plants. But, because has implications for population establishment and persistence, range many species exhibit a seed size–seed number trade- off (Fenner expansions, and evolutionary potential across the range (Forsman, & Thompson, 2005), the use of a single trait value to characterize 2014); however, such co- occurring scale- dependent patterns of vari- fecundity might overlook meaningful biology relevant to a species’ ation are rarely documented (but see Délye et al., 2010). ability to establish new populations or persist once established. And Weedy and invasive species should be particularly useful for because large seeds are often better able to sustain developing seed- investigating patterns of morphological variation and adaptation at lings in the presence of competing vegetation than are small ones multiple spatial scales. Because many such species are geographi- (Leishman, Wright, Moles, & Westoby, 2000), it may be adaptive for cally widespread and occur in a range of distinct habitats (e.g., plants growing in dense vegetation to produce large seeds—even if Nelson & Anderson, 2015), they should experience a complicated this means producing fewer of them. The general lack of knowledge mosaic of selection pressures. Many weedy and invasive species about intraspecific trait variation in weedy and invasive species thus also harbor substantial genetic and/or phenotypic variability at the represents a major gap in understanding the ecology of these groups population level (Clements et al., 2004; Dlugosch & Parker, 2008; and a potential “Achilles heel” in our ability to predict their adaptive Lavergne & Molofsky, 2007; Vigueira, Olsen, & Caicedo, 2013; responses to changing conditions. Warwick, Thompson, & Black, 1987), making it possible that spatial The weedy species giant ragweed (Ambrosia trifida, Asteraceae) patterns of selection could yield corresponding patterns of phe- provides a compelling system for investigating morphological varia- notypic variation. Further, spatial patterns in phenotypic variation tion across multiple spatial scales. Giant ragweed is a wind- pollinated may repeat across the landscape, especially when species exist in and mostly outcrossing species that is native to North America commonly occurring environments with unique selection pressures (Bassett & Crompton, 1982) and can be found throughout much of such as agricultural fields, roadsides, and other highly disturbed the continent (Payne, 1970). The species is highly variable morpho- areas (Lee & Gelembiuk, 2008; Vigueira et al., 2013). And, because logically and genetically (Abul- Fatih, Bazzaz, & Hunt, 1979; Patzoldt range expansions and postintroduction population dynamics are in- & Tranel, 2002; Sako et al., 2001); thus, we expect it should respond herently variable, populations from different parts of the weedy or to variable selection pressures across the range. In its native habi- invasive range may differ in their responses to selective pressures or tats, giant ragweed generally occurs in early- successional and dis- the strength of selection. turbed sites with moist soils (Bassett & Crompton, 1982), although it Of course, despite the many reasons one might expect weedy also occurs in drier upland sites (Regnier et al., 2016). Giant ragweed and invasive species to exhibit complex patterns of phenotypic vari- is also a
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