TESTING DARWIN’S NATURALIZATION CONUNDRUM BASED ON TAXONOMIC,
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PHYLOGENETIC AND FUNCTIONAL DIMENSIONS OF VASCULAR PLANTS
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Jesús N. Pinto-Ledezma
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, Fabricio Villalobos
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, Peter B. Reich
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, Daniel J. Larkin
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,
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Jeannine Cavender-Bares
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Department of Ecology, Evolution and Behavior, University of Minnesota, 1479 Gortner Ave,
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Saint Paul, MN 55108, USA
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Instituto de Ecología, A.C., Red de Biología Evolutiva, Carretera antigua a Coatepec 351, El
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Haya, 91070 Xalapa, Veracruz, México
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Department of Forest Resources, University of Minnesota, 1530 Cleveland Ave, Saint Paul, MN
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55108, USA
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Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South
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Wales 2753, Australia;
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Department of Fisheries, Wildlife, and Conservation Biology, University of Minnesota, 135
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Skok Hall, 2003 Upper Buford Circle, Saint Paul, MN 55108, USA
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*Corresponding Author: jpintole@umn.edu, jesuspintoledezma@gmail.com
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Running Header: Dissecting Darwin’s naturalization conundrum
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Keywords: Cedar Creek, community phylogenetics, co-occurrence patterns, invasion dynamics,
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fire frequency, focal-species, functional traits, limiting similarity, long-term oak savanna
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experiment, species sorting
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not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available
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not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available
The copyright holder for this preprint (which wasthis version posted November 20, 2019. ; https://doi.org/10.1101/847442doi: bioRxiv preprint
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not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available
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Abstract
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Charles Darwin posited two alternative hypotheses to explain the success of nonnative species
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based on their relatedness to incumbent natives: coexistence between them should be (i) more
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likely with greater relatedness (due to trait similarity that correlates with better matching to the
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environment), or (ii) less likely (due to biotic interference, such as competition). The paradox
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raised by the opposing predictions of these two hypotheses has been termed ‘Darwin’s
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naturalization conundrum’ (DNC). Using plant communities measured repeatedly over a 31-year
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time span across an experimental fire gradient in an oak savanna (Minnesota, USA) we evaluated
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the DNC by explicitly incorporating taxonomic, functional and phylogenetic information. Our
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approach was based on ‘focal-species’ such that the taxonomic, functional and phylogenetic
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structure of species co-occurring with a given nonnative species in local communities was
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quantified. We found three main results: first, nonnatives colonizers tended to co-occur most
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with closely related incumbent natives in recipient communities, except in the extreme ends of
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the fire gradient (i.e., communities with no fire and those subjected to high fire frequencies);
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second, with increasing fire frequency, nonnative species were functionally more similar to
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native species in recipient communities; third, functional similarity of co-occurring nonnatives
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and natives in recipient communities showed a consistent pattern over time, but the phylogenetic
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similarity shifted over time, suggesting that external forces (e.g., climate variability) are also
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relevant in driving the phylogenetic relatedness of nonnatives to natives in invaded communities.
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Our results provide insights for understanding the invasion dynamics across environmental
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gradients and highlight the importance of evaluating different dimensions of biodiversity in order
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to produce more powerful evaluations of species co-occurrence at different spatial and temporal
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scales.
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Introduction
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The assembly and maintenance of ecological communities is a dynamic process operating over
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multiple spatial and temporal scales, that incorporates local niche-based interactions and sorting
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to stochastic and historical processes that may operate over large spatial scales (Tilman 2004,
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Cavender-Bares et al. 2009, 2018a, Pinto-Ledezma et al. 2019). Over the past millennium,
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human activities have greatly influenced these natural processes, through habitat degradation and
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biological invasions by moving species out of their native ranges, with negative consequences
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for biodiversity, ecosystem functioning, and human well-being (Sax et al., 2007, Thuiller et al.
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2010, Vilà et al. 2011, Simberloff et al. 2013, Capinha et al. 2015).
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Given the importance of biological invasions in determining current community structure
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(Pearson et al. 2018), understanding the causes of invasion success have become a major goal in
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ecology, evolution and conservation (Dawson et al. 2017). While there are many competing
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hypotheses for the success and failure of colonizing species (Blumenthal 2005, Jeschke et al.
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2012, Jeschke 2014, Prins and Gordon 2014), two major hypotheses have been proposed as
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explanations for species invasion success that incorporate evolutionary relatedness as a primary
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consideration (Gallien and Carboni 2017, Ma et al. 2016, Cadotte et al. 2018). First, Darwin’s
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naturalization hypothesis (DNH; Box 1: Fig. 1A) suggests that nonnative species closely related
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to resident natives are less likely to invade native assemblages because the niches they could
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invade are already occupied by ecologically similar relatives (Daehler 2001). In contrast, the pre-
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adaptation hypothesis (PAH; Box 1: Fig. 1B) postulates that nonnative species closely related to
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resident natives should be favored precisely because of their niche similarity with native species,
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sharing traits that make them well-suited to the novel range (Ricciardi and Mottiar, 2006).
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Accordingly, the extent to which nonnative species are closely or distantly related to resident
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species may teach us whether competitive interactions or environmental filters, respectively, are
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dominant factors determining invasion success (Gallien and Carboni 2017, Cadotte et al. 2018).
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These opposing hypotheses both trace back to Darwin (1859) and together comprise ‘Darwin’s
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naturalization conundrum’ (DNC, Diez et al. 2008, Thuiller et al. 2010, Cadotte et al. 2018).
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Deciphering the connection between ecological and evolutionary processes in driving
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species distributions and the assembly of communities is crucial to understand the invasion
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success of nonnative species in recipient communities (Gallien and Carboni 2017, Cadotte et al.
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2018, Pearson et al. 2018). Although the DNC represents an integrative explanation that links
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both ecological and evolutionary processes (reviewed in Cadotte et al. 2018), invasion is a
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dynamic process, i.e., nonnative species are continually expanding or retracting their
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geographical ranges across the regions they have recently colonized (Sax et al. 2007, Blackburn
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et al. 2015, Pannell 2015). Thus, the presence of nonnative species in a community does not
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necessarily indicate that they are optimally-adapted to the new environmental or niche
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conditions. One potential explanation for the spread of invasive species is the ‘ecological fitting
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hypothesis’ (EFH, Janzen 1985), which suggests that widespread species can occupy new places
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or environmental conditions without being perfectly adapted to them (Janzen 1985, Cavender-
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Bares et al. 2018b, but see Odour et al. 2016). In addition, functional traits underlie composition,
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community assembly and ecosystem processes (Cavender-Bares et al. 2009, Cavender-Bares et
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al. 2016, Lavorel et al. 2011, Reich 2014, Catford et al. 2019); thus, different functional traits or
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trait combinations can modulate the degree to which nonnative species are able to colonize and
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further adapt to the ecological conditions found in recipient communities (Blumenthal 2005, van
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Kleunen et al. 2010, Carboni et al. 2018; Catford et al 2019). Recent evidence suggests that
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successful invasive species tend to have higher values for traits associated with resource
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acquisition, dispersal, and establishment and competitive ability than local native species (van
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Kleunen et al. 2010, Carboni et al. 2018, Catford et al. 2019), indicating that they have similar or
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higher performance in the novel range than native species (Sax et al. 2007, Odour et al. 2016, but
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see González-Muñoz et al. 2014).
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Several studies have evaluated the DNC across different spatial scales and systems (for a
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review see Cadotte et al. 2018, Gallien and Carboni 2017, Ma et al. 2016). However, few studies
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have explored the dynamics of species composition and relatedness within communities during
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the invasion process (Blackburn et al. 2015, Li et al. 2015) or the role of functional traits in
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modulating colonization and establishment by nonnative species (Marx et al. 2015, Carboni et al.
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2018; but see Catford et al 2019). Although these studies have generally found similar results—
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from a phylogenetic perspective, nonnative species tend to coexist more with their close relatives
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(e.g., Li et al. 2015, Marx et al. 2015, Kusumoto et al. 2019)—the incorporation of functional
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information into analyses provides new insights regarding functional differentiation between
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coexisting species (Cavender-Bares et al. 2009, Cadotte et al. 2018); and consequently a way
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forward to understand how species’ ecological differences regulate the colonization,
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establishment and persistence of nonnative species within local native communities across
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spatial and temporal scales.
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Here, using plant communities sampled over decades across an experimental fire gradient
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at Cedar Creek Ecosystem Science Reserve (hereafter Cedar Creek) in Minnesota, USA, we
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evaluate the DNC while explicitly incorporating taxonomic, functional, and phylogenetic
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information into our analyses. To do so, we apply a novel approach based upon the framework of
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Villalobos et al. (2013, 2017), extending the concept of species’ functional/phylogenetic fields—
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the overall functional/phylogenetic structure within a given species’ geographical range—to
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.CC-BY-NC-ND 4.0 International licenseunder a
not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available
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