*Shared first authorship
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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.