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The Role of Diversification in Community Assembly of the Oaks (Quercus L.) Across the Continental U.S

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The Role of Diversification in Community Assembly of the Oaks (Quercus L.) Across the Continental U.S RESEARCH ARTICLE INVITED SPECIAL ARTICLE For the Special Issue: Using and Navigating the Plant Tree of Life The role of diversification in community assembly of the oaks (Quercus L.) across the continental U.S. Jeannine Cavender-Bares1,7, Shan Kothari2,7, José Eduardo Meireles1,7, Matthew A. Kaproth1,4, Paul S Manos3, and Andrew L. Hipp5,6 Manuscript received 4 July 2017; revision accepted 20 December PREMISE OF THE STUDY: Evolutionary and biogeographic history, including past environmental 2017. change and diversification processes, are likely to have influenced the expansion, migration, 1 Department of Ecology, Evolution and Behavior, University of and extinction of populations, creating evolutionary legacy effects that influence regional Minnesota, 1479 Gortner Avenue, St. Paul, MN 55108, USA species pools and the composition of communities. We consider the consequences of 2 Department of Plant Biology, University of Minnesota, 1479 the diversification process in shaping trait evolution and assembly of oak-dominated Gortner Ave, St. Paul, MN 55108, USA communities throughout the continental United States (U.S.). 3 Department of Biology, Duke University, Durham, NC 27708, USA METHODS: Within the U.S. oaks, we tested for phylogenetic and functional trait patterns at 4 Department of Biological Sciences, Minnesota State University, different spatial scales, taking advantage of a dated phylogenomic analysis of American oaks Mankato, MN 56001, USA and the U.S. Forest Service (USFS) Forest Inventory and Analysis (FIA). 5 The Morton Arboretum, 4100 Illinois Route 53, Lisle, IL 60532, USA KEY RESULTS: We find (1) phylogenetic overdispersion at small grain sizes throughout the 6 The Field Museum, 1400 S Lake Shore Drive, Chicago, IL 60605, U.S. across all spatial extents and (2) a shift from overdispersion to clustering with increasing USA grain sizes. Leaf traits have evolved in a convergent manner, and these traits are clustered in 7 Authors for correspondence (e-mails: [email protected], communities at all spatial scales, except in the far west, where species with contrasting leaf [email protected], [email protected]) types co- occur. Citation: Cavender-Bares, J., S. Kothari, J. E. Meireles, M. A. Kaproth, P. S Manos, and A. L. Hipp. 2018. The role of diversification CONCLUSIONS: Our results support the hypotheses that (1) interspecific interactions were in community assembly of the oaks (Quercus L.) across the continen- important in parallel adaptive radiation of the genus into a range of habitats across the tal U.S. American Journal of Botany 105(3): 565–586. continent and (2) that the diversification process is a critical driver of community assembly. doi:10.1002/ajb2.1049 Functional convergence of complementary species from distinct clades adapted to the same local habitats is a likely mechanism that allows distantly related species to coexist. Our findings contribute to an explanation of the long- term maintenance of high oak diversity and the dominance of the oak genus in North America. KEY WORDS community assembly; complementarity; convergent evolution; diversification processes; environmental sorting; evolutionary legacy effects; functional traits; phylogenetic structure; species interactions; sympatric parallel adaptive radiation. The integration of phylogenetic biology and functional ecology into to ecosystem restoration in the face of widespread anthropogenic the study of biological communities has helped in deciphering the disturbance (Cavender- Bares and Cavender, 2011; Hipp et al., processes that shape community assembly (Webb et al., 2002; Kraft 2015; Barak et al., 2016). While competitive interactions and en- et al., 2007; Vamosi and Vamosi, 2007; Cavender- Bares et al., 2009; vironmental sorting processes have been highlighted as critical to Kraft and Ackerly, 2010; Eaton et al., 2012; Hawkins et al., 2014). local community assembly (Weiher and Keddy, 1999a; Webb et al., These advances are critical to understanding the predictability of 2002), diversification and long- term evolutionary and biogeo- ecosystem composition under global change and highly relevant graphic processes remain underappreciated in understanding local American Journal of Botany 105(3): 565–586, 2018; http://www.wileyonlinelibrary.com/journal/AJB © 2018 Botanical Society of America • 565 566 • American Journal of Botany community assembly (Gerhold et al., 2015). The role of historical resource- conservative trait values are advantageous in resource- processes in the assembly of plant communities remain understud- limited environments (Chabot and Hicks, 1982; Kikuzawa, 1995; ied, despite the known importance of adaptive radiation and histor- Reich, 2014). Furthermore, biotic interactions involving facilitation ical colonization patterns in the assembly of island and continental are frequently overlooked in hypothesized consequences of species floras (Pennington et al., 2004, 2009; Ricklefs, 2004; Emerson and interactions for community structure (Valiente- Banuet and Verdú, Gillespie, 2008; Crisp et al., 2009; Fine, 2015). Here we examine 2007). While phylogenetic overdispersion is frequently attributed the functional and phylogenetic structure of oak- dominated tree to competitive exclusion or other density-dependent processes un- communities from local to continental scales to examine the con- der the umbrella of biotic interactions, both empirical and simu- sequences of evolutionary and historical processes in shaping the lation studies have shown that it can be caused by habitat sorting composition and diversity of North American oak forest communi- processes and environmental filtering if critical functional traits ties. Our goal is to link deep- time processes to current patterns in that influence distributions are convergent (Cavender- Bares et al., an effort to understand why the oaks have unusually high local and 2004b; Kraft et al., 2007). Understanding why traits may be conver- continental diversity and abundance. gent ultimately requires knowledge of diversification. The phylogenetic structure of co- occurrence patterns is a cu- The processes that dominate community assembly vary with mulative consequence of historical processes, such as speciation, spatial scale (Weiher and Keddy, 1999b; Laliberté et al., 2009) and extinction, and dispersal (Kembel, 2009; Villalobos et al., 2013), thus lead to shifting expectations of phylogenetic and trait structure ecological interactions and genetic processes, such as disease in communities (Cavender- Bares et al., 2006; Swenson et al., 2006, (Gilbert and Webb, 2007) and pest (Mouillot et al., 2005; Lind 2007; Willis et al., 2010; Brunbjerg et al., 2014; Yan et al., 2016). et al., 2015) dynamics, introgression (Eaton et al., 2015; Pollock Grain size and spatial extent are two distinct but important compo- et al., 2015), competition (Davies et al., 2007; Cooper et al., 2008), nents of spatial scale (Turner et al., 2001) that are expected to have facilitation (Valiente- Banuet and Verdú, 2007), and environmental different consequences for community structure. A community as- sorting (Helmus, 2007; Savage and Cavender-Bares, 2012; Swenson semblage is defined by the grain size (i.e., the plot size of an observed et al., 2012) (Box 1). Over long timescales, ecological processes and assemblage) that we choose, while comparisons among assemblages introgression surely influence evolutionary dynamics and diversi- and the pool of species that we assume those assemblages are de- fication, shaping the radiations of important lineages and their on- rived from depend on the spatial extent that we circumscribe for going community assembly processes (Van Valen, 1976; Schluter, the analysis. At small grain sizes, our focal species can be assumed 2000; Ricklefs, 2007; Tyerman et al., 2008; Givnish et al., 2009; to interact (or potentially interact) directly, and environmental con- Keller et al., 2013; Cannon and Lerdau, 2015). Historical diversi- ditions may be relatively homogeneous, whereas at increasing grain fication processes have also influenced the evolution of functional sizes individuals within the assemblage would be less likely to inter- traits, thus influencing the extent to which closely related species act directly, although environmental variation may increase among are adapted to similar or contrasting habitats. At shorter times- assemblages, depending on the scale of variation of the most critical cales, density- dependent ecological processes and environmental environment axis. Keddy and Weiher (1999) thus hypothesized that selection pressures drive the co- occurrence patterns and sorting of biotic interactions should have greater importance at smaller spatial species into habitats. Yet the functional traits of organisms that are scales, whereas environmental adversity should influence assembly mechanistically linked to these processes reflect their longer-term more strongly at larger spatial scales. evolutionary history. Phylogenetic similarity can be used proximally as an integrated A persistent challenge is to tease apart the influence of multi- measure of functional similarity and can stand in for unmeasured ple processes interacting in complex ways to shape the structure of traits (Cadotte et al., 2009, 2011). Phylogenetic similarity is com- species assemblages (Lessard et al., 2015), given that there are more pellingly linked to similarity in susceptibility to disease (Webb potential processes that may account for the structure of species as- et al., 2006; Gilbert and Webb, 2007) and
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