Deconstructing Darwin's Naturalization Conundrum in the San Juan Islands using community phylogenetics and functional traits

Abstract

Aim Darwin posed a conundrum about species invasions, postulating the importance of functional distinctiveness from the receiving native community to avoid competition, and, at the same time, the importance of shared similarity to pass environmental filters and successfully establish. Using phylogenetic distances and functional traits, we assessed this conundrum in the flora of 80 mostly uninhabited islands, where over 30% of the species are invasive. We highlight the importance of publicly available datasets to disentangle ecological processes that may drive invasion. Location San Juan Islands archipelago, Pacific Northwest of North America. Methods Using a supermatrix approach, we inferred a maximum‐likelihood estimate of the mega‐phylogeny for the vascular plants on the San Juan Islands. We gathered measurements for five ecologically relevant functional traits – seed mass, maximum height, specific leaf area, leaf size and leaf nitrogen content. We assessed phylogenetic and functional trait similarity between invasive species and the receiving native community, and tested the significance of the observed patterns against a randomly generated invading community. Results Invasive species were more closely related (phylogenetically clustered) to their nearest native than natives were on 40 of the islands and were more clustered than any random invasive in the species pool on 22 islands. Despite phylogenetic similarity, functional traits differed between the two status groups, at least for maximum height and specific leaf area. When comparing functional differences between phylogenetically close relatives, more complex patterns emerge. Main conclusion Only with the combination of both evolutionary history and phenotypic traits were we able to discover support for both sides of Darwin's conundrum – although invasive species have phylogenetically close native relatives, functional traits differ between the two status groups. This implies that both environmental filtering and competitive interactions may be important for invasion success in this archipelago.

Comparing traits of native and alien plants: Can we do better?

“…The infrequent application of such approaches (Cross et al., ; Dainese & Bragazza, ) suggests we are still a long‐way from developing robust generalisations about plant invasions. For example, comparisons of trait differences between native and alien species are still undertaken at regional scales (Bezeng, Davies, Yessoufou, Maurin, & Van der Bank, ; Kuester, Conner, Culley, & Baucom, ; Marx, Giblin, Dunwiddie, & Tank, ) even though the relevance of such analyses for understanding the vulnerability of plant communities to plant invasion is debatable. The increasing availability of plot‐scale data world‐wide (Chytry et al., ; Rutherford, Mucina, & Powrie, ; Walker et al., ) has the potential to herald considerable new insights into the role that trait differences between native and alien species may play in plant invasions and facilitate the application of methods that account for spatial scale dependence, environmental gradients and even temporal variation in species composition.…”

The community ecology of invasive species: where are we and what's next?

“…In contrast, most studies exploring the effects of phylogenetic relatedness between invasives and natives on community resistance (i.e. phylogenetic species‐based indices) have yielded mixed (Jones et al , Liu et al , Poe , Lososová et al , Marx et al ) or non‐significant results (Castro et al , Fleming et al ). Nevertheless, a recent study by Tan et al () in a manipulative experiment with bacterial assemblages found evidence that phylogenetic relatedness to invaders was a better predictor of biotic resistance than the phylogenetic diversity of the community.…”

“…Schaefer et al (2011), Park and Potter (2013, 2015a,Li et al (2015a),Marx et al (2016) Ranked difference indices The standardized mean differences in trait values between the invader and each native species in the community.…”

Testing Darwin's Naturalization Conundrum using phylogenetic relationships: Generalizable patterns across disparate communities?

“…Therefore, overall, our study shows that while patterns of phylogenetic relatedness among non-native and native species within a community can offer insight into a community's susceptibility to invasion, phylogenetic relatedness alone may be an insufficient predictive tool for understanding the rules of community assembly. Rather, future efforts integrating phylogenetic diversity with other measures, such as phenotypic traits (e.g., Gaynor, Ng, & Laport, 2018;Marx et al, 2016;Schaefer et al, 2011), and abiotic factors (e.g., Lim, Crawley, De Vere, Rich, & Savolainen, 2014;Qian & Sandel, 2017), will help elucidate whether phylogenetic relatedness together with other factors can be used to predict a community's susceptibility to the establishment of new species.…”

“…Although many early studies used taxonomy-based metrics of species relatedness following Darwin (e.g., comparing generic affinities), the increased availability of sequence data and computing power has led to a rise in the number of studies testing DNC with metrics that quantify relatedness from phylogenetic relationships (Gerhold et al, 2011;Strauss, Webb, & Salamin, 2006;Tan, Pu, Ryberg, & Jiang, 2015). These studies have revealed that the process of community assembly is more complicated than previously thought, with different studies providing support for both alternatives of DNC (reviewed in Thuiller et al, 2010;Jones, Nuismer, & Gomulkiewicz, 2013;Ma et al, 2016;Marx, Giblin, Dunwiddie, & Tank, 2016). The lack of a general pattern appears to be largely due to studies differing in temporal scale (i.e., stage of invasion) (Li et al, 2015;Ma et al, 2016), spatial scale (e.g., local versus regional) (Carboni et al, 2013;Davies, Cavender-Bares, & Deacon, 2011;Ma et al, 2016;Schaefer, Hardy, Silva, Barraclough, & Savolainen, 2011) and/or phylogenetic scale (Procheş, Wilson, Richardson, & Rejmánek, 2008;Thuiller et al, 2010).…”