Reconciling Darwin’s naturalization and pre‐adaptation hypotheses: An inference from phylogenetic fields of exotic plants in Japan

Abstract

Aim Understanding the causes and consequences of biological invasions remains a challenge for several disciplines, including biogeography. One major issue in overcoming this challenge is disentangling the confounding mechanisms of species invasiveness and community invasibility. Here, we tackle this issue by applying a novel approach based on the phylogenetic affinities between exotic species and natives in the recipient community to elucidate naturalization and pre‐adaptation processes. Location Japan. Taxon Seed plants. Methods Geographical co‐occurrence data for 1,094 exotics and 4,869 native species (including 1,676 endemics) were created at the 10‐km grid‐cell and vegetation‐plot levels. For individual exotic species, standardized effect size of phylogenetic species variability (PSVSES) of the recipient native assemblage (i.e. phylogenetic fields) was calculated and its clustering/over‐dispersion was tested, representing exotic invasiveness in relation to invasibility of native recipients. To identify drivers of species invasiveness, the correlation of PSVSES with species attributes, involving phylogenetic distance between each exotic and native species, was explored. Results Phylogenetic fields (PSVSES) showed significant over‐dispersion (~16% exotics) or clustering (~14% exotics). Interspecific variation of PSVSES among exotics was substantially explained by species ecological attributes. Geographical extent and climatic niche widths were negatively correlated with PSVSES. Preference for human influence was positively correlated with PSVSES at the 10‐km grid‐cell level, but negatively at the vegetation‐plot level. Exotics colonized from the Palearctic and Indo‐Malay regions, which belong to the same biogeographical region as East Asia, tended to have clustered phylogenetic fields. Main conclusions Environmental filtering and biotic sorting both played a key role in exotic plant colonization, supporting both of Darwin's contradictory hypotheses of naturalization versus pre‐adaptation. Clustered phylogenetic fields indicated that an exotic colonizes its recipient assemblage through abiotic filtering (i.e. pre‐adaptation); at the same time, phylogenetic over‐dispersion was indicative of naturalization for exotics that occupied a biotic niche space among native recipients (i.e. naturalization). Phylogenetic field patterns depended on species’ ecological attributes, including phylogenetic relatedness between exotics and recipient natives, especially reflecting invasibility at the local‐community level.

Testing Darwin’s naturalization conundrum based on taxonomic, phylogenetic, and functional dimensions of vascular plants

“…Multiple processes have been proposed to explain introduced species' success outside their native ranges (Gallien and Carboni 2017, Cadotte et al 2018, Redding et al 2019. Prior studies have reported contrasting results in terms of phylogenetic relatedness of nonnative species to recipient assemblages (Carboni et al 2013, Li et al 2015, Marx et al 2016, with mixed support for both hypotheses comprising Darwin's naturalization conundrum (Kusumoto et al 2019). Our results show differential patterns of relatedness of focal nonnative species to recipient native communities, with some nonnatives co-occurring more with closely related natives (supporting the pre-adaptation hypothesis), and others with distantly related natives (supporting the naturalization hypothesis; Figs.…”

“…Although there has been considerable research into traits associated with species invasiveness (van Kleunen et al 2010), relatively few studies have explicitly considered the role of functional traits in mediating colonization, establishment (Carboni et al 2018, Catford et al 2019, and long-term persistence (Marx et al 2016, Catford et al 2019 of nonnative species in local communities. Although several recent studies have generally found similar results (from a phylogenetic perspective, nonnative species tend to coexist more with their close relatives; e.g., Li et al 2015, Marx et al 2016, Williams et al 2018, Kusumoto et al 2019, the incorporation of functional information into analyses provides new insights regarding functional differentiation between coexisting natives and nonnative species (Cavender-Bares et al 2009, Cadotte et al 2018.…”

Integrating multiple sources of ecological data to unveil macroscale species abundance

“…The vegetation would probably have changed, however, at least due to recent environmental changes, such as the increase of herbivorous animals (e.g. deer 43 ) and the spread of introduced species 44,45 . Using the dataset for a specific time period may better reflect the species abundance at a certain point of time, but at the expense of reduced sample size.…”

Factors influencing the precision of species richness estimation in Japanese vascular plants

“…Species names followed the Japanese Scientific Names Index (Yonekura & Kajita, 2003). In this analysis, exotic species including planted species were excluded from the dataset (Kusumoto et al, 2019). Kubota et al (2015), Kubota et al (2017) provided a more detailed description of how this dataset was created.…”

“…Here, we try to fill this gap in our knowledge using the distributional data (presence-absence) of Japanese plant species as a model system. This dataset contains complete information on the occurrence of each Japanese plant species at the 10 × 10 km grid cell level (Kusumoto, Villalobos, Shiono, & Kubota, 2019). Thus, our data do not rely on samples, but on complete censuses.…”