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Name and complete mailing address of the person to whom correspondence should be sent: Daniel Sol, CREAF-CSIC, Cerdanyola del Vallès, Catalonia E-08193, Spain. TEL: +34 93-5814678. E-MAIL: d.sol@creaf.uab.cat
Author contributions: DS, JGC and CGL conceived and designed the study; DS, CGL, ALP, JAT and CT collected data; DS and JGP conducted the analyses; DS wrote the manuscript and all authors edited and approved it.
Data accessibility statement: We confirm that, should the manuscript be accepted, the data supporting the results will be archived Dryad, and the data DOI will be included at the end of the article.
Abstract. Despite biological invasions are one of the main environmental problems of the twenty-first century, there is still no theoretical or empirical agreement on whether a high phylogenetic relatedness between exotic and native species positively or negatively affect invasion success. To resolve this conundrum, it has been proposed that the effect might be scale-dependent, being negative at smaller spatial scales and positive at larger scales. Here we show that this scale-dependent pattern may be a sampling artefact associated with species-area effects and a non-random pattern of species introductions. We support this conclusion with simulations and empirical data on invaded and non-invaded avian communities in regions from five continents. We further show that at smaller-scales —where these artifacts are negligible— invasion success generally increases with the presence of closely-related species, but that predictive accuracy largely depends on considering the influence of human-related disturbances in facilitating invasions.
Keywords: Biotic resistance; environmental filtering; invasion potential; risk assessment; alien species
Growing concern over the environmental and socio-economic impact of biological invasions has fueled a surge of interest in identifying and preventing situations where the risk of a species becoming invasive is high (Hulme et al. 2008; Blackburn et al. 2009; Pyšek & Richardson 2010; Pysek et al. 2010; Li et al. 2015). However, anticipating these situations has proved challenging, primarily because the risk of invasion depends not only on the features of the exotic species but also on the way they interact with the species from the recipient community (Shea & Chesson 2002; Duncan et al.2003; Romanuk et al. 2009). A potential way to tackle this challenge was proposed by Darwin (Darwin 1859) who suggested that the degree of evolutionary relatedness between exotic and native species can inform the likelihood that a species establishes and proliferates (i.e. becomes invasive). If invasion success were related to evolutionary relatedness, this would not only allow a more accurate assessment of the risk of biological invasions but also assess the risk for species that are data-deficient regarding their ecology or success in previous introductions.
Although Darwin’s suggestion has attracted increased research attention, there is still no empirical agreement on whether relatedness to native species positively or negatively influences invasion success (Cadotteet al. 2018). In fact, both possibilities are predicted by theory (Darwin 1859; Daehler 2001; Thuiller et al. 2010; Cadotteet al. 2018). Darwin’s naturalization hypothesis suggests that introduced species should be less successful at invading communities in which their close relatives are present, because phylogenetically-related species often share similar niches and hence are more likely to compete for similar resources. Thus, the hypothesis predicts a negative association between relatedness to native species and invasion success. However, if successful invasion instead primarily depends on phylogenetically-conserved adaptations to find a suitable niche in the novel environment, then the presence of close-relatives may indicate that the invader already has the necessary adaptations (hereafter ‘preadaptation hypothesis’). This predicts a positive association between relatedness to native species and invasion success.
Both the naturalization and preadaptation hypotheses are theoretically sound and have been demonstrated in small-scale experiments (Jianget al. 2010; Li et al. 2015), but extrapolating the results to the real world has proven difficult, with multiple studies reporting contradictory results (Cadotte et al. 2018). Discrepancies among studies may reflect methodological shortcomings (Thuiller et al. 2010; Li et al. 2015). These include inaccurate assessment of invasion success, insufficient phylogenetic resolution, inappropriate spatial scales of analysis and violation of the assumption of statistical independence when making inference (Lambdon & Hulme 2006; Diez et al. 2008; Thuiller et al.2010; Sol et al. 2014b; Li et al. 2015). Thuiller et al. (2010), for example, suggested that large spatial scales and taxonomy-based relatedness metrics are unlikely to detect the signature of competition and hence are inappropriate to test the naturalization hypothesis. These authors advocate for quantifying relatedness based on the phylogenetic distance between exotic and local native species as a stronger framework to link invader characteristics and community properties. The key assumption that phylogenetic distance correlates with ecological distance is also contentious, largely because the strength of niche conservatism is known to vary across clades (Wienset al. 2010). Evaluating this assumption empirically requires not only testing whether phylogenetic relatedness describes the degree of niche overlap in resource use—a fundamental premise of the naturalization hypothesis—but also whether it describes the extent to which close relatives share the traits required to thrive in a particular environment, a major assumption of the preadaptation hypothesis.
The ecological context is also critical to reconciling the opposing predictions regarding the relationship between phylogenetic distance and invasiveness. Specifically, the naturalization hypothesis assumes that competition controls community composition. While competition can certainly prevent the success of some introduced species (Levineet al. 2004), whether this is the primary mechanism controlling biological invasions remains controversial. One reason is that many exotic species attain higher success in human-altered environments, where competitive regimes may have been changed by frequent disturbances and the extirpation of many native species (Elton 1958; Bartomeuset al. 2012; Cadotte et al. 2017; Sol et al.2017b). In these environments, the success of the species may largely depend on the ability of individuals to cope with new challenges to which they have had little opportunity to adapt, potentially favoring preadapted species (Sol & Maspons 2016; Sol et al. 2017b). However, previous attempts to reconcile the naturalization and preadaptation hypotheses have focused on the influence of the spatial scale of analysis rather than on the environmental contexts where either competition or filtering should be more relevant. Park et al. (Parket al. 2020), for example, recently suggested that at small spatial scales, competitive exclusion inhibits alien invasions, but these effects are attenuated at larger spatial scales because of greater environmental heterogeneity. Thus, spatial scale provides an alternative solution to Darwin’s naturalization conundrum.
Here, we provide an empirical assessment of Darwin’s naturalization conundrum for birds. A recent analysis by Redding et al. (Reddinget al. 2019) revealed that the biotic environment had a relatively weak effect on establishment success of birds compared to other factors such as propagule pressure or the species’ life history. After accounting for these other factors, however, the probability of establishment increased with the presence of closely related species in the region. While these findings are consistent with the preadaptation hypothesis, it remains to be shown whether and how the phylogenetic structure of the recipient communities influences the success of invaders once established. This is a crucial gap, because the impact of exotic species largely depends on the extent to which the species increases in numbers and expands across different habitats.
Using published data on well-surveyed avian communities along gradients of human-related disturbances (Sol et al. 2020b), we assess whether phylogenetic relatedness to native species predicts invasion success, and whether the predictive power varies with the scale of analysis and/or the degree human-related disturbances. Our analyses are based on > 1,300 estimations of invasion success for 63 exotic species —including all the most invasive birds and invaded regions worldwide (Dataset 1). Because the same species was frequently introduced to different locations, and because most locations were subject to several introductions and contained communities with different species and exposed to different levels of disturbance (Fig. 1 ), our dataset provides a unique opportunity to clarify Darwin’s naturalization conundrum. In addition, we make use of the increased availability of avian functional trait data sets describing fine-scale variation in trophic niche, resource acquisition behaviors and response to novel environments (Pigot et al. 2020; Solet al. 2020b), allowing us to go beyond a mere assessment of phylogenetic relatedness between invaders and their community neighbors to assess whether phylogenetic patterns reflect ecological differences.