Results and Discussion
Our analyses do not support that the probability of observing the
signature of environmental filtering and competition is scale-dependent
(Park et al. 2020). We found that the phylogenetic distance of
exotic species to the closest coexisting native relative was, on
average, three times larger at the local community level than at the
continental level (Fig. 2A ), consistent with previous studies
(Park et al. 2020). Yet a similar pattern was found when we
instead estimated the minimum phylogenetic distance between each exotic
species and the native species from communities where those exotic
species are absent (Fig. 2B ). Thus, it is unlikely that the
pattern is a signature of environmental filtering. A more plausible
alternative is that the increase in species richness at larger spatial
scales increases the probability of including a closely related exotic
and native species (Fig. 2C ).
Given the risk that results are biased by sampling artifacts, we opted
by addressing the conundrum at lower spatial scales and ask whether the
success of the invader in a community is influenced by the degree of
phylogenetic relatedness with native neighbors. Under the naturalization
hypothesis, for example, we should expect that within any region exotic
species will be restricted to those communities where they do not find
close relatives. Instead, the preadaptation hypothesis predicts a
preference for communities with close relatives. As some exotic species
were absent from certain communities despite being well-established in
near-by communities (505 out of 1,359 cases), we tested whether the
probability that an exotic species occurred in a community was related
to the phylogenetic distance with the native species from the community.
Despite previous studies suggesting that the naturalization hypothesis
should be favored at smaller spatial scales, we found no evidence that
the presence of close relatives competitively exclude exotic species. On
the contrary, we found that exotic species were more likely to be
present in communities containing native species that are on average
more closely related (Fig. 3A, B ).
One possible explanation for the failure to support the naturalization
hypothesis is that native species may reduce the success of exotic
species but rarely prevent invasion (Levine et al. 2004). Thus,
the relative abundance of an exotic species in the community may be a
more informative measure of invasion success to address the
naturalization hypothesis. Based on estimations of exotic species
abundance in communities where they were established (N = 792), we again
found no evidence that exotic species more distantly related to native
residents reach higher relative abundances than exotic species with
closer relatives (Fig 3C, D ). Rather, exotic species abundances
marginally decreased with the mean and nearest phylogenetic distance to
native species. Although most native species in the studied communities
had low relative abundances (Sol et al. 2020b), and thus may be
unlikely to inhibit invasions even if the exotic species have similar
resource needs, the conclusion does not change when using mean and
nearest phylogenetic distances weighted by their relative abundance
(Fig 3E-H ).
The lack of support for the naturalization hypothesis may reflect that
in birds competition plays a minor role in influencing invasion success,
relative to other intrinsic or environmental factors (Duncan et
al. 2003). One reason is that exotic species tend to attain higher
success in disturbed habitats, mostly urbanized habitats (Sol et
al. 2020b), where competitive regimes have frequently been altered by
the extinction of native species (Bartomeus et al. 2012). These
human-altered habitats often impose strong environmental filtering, as
only a few species have the adaptations needed to live in artificial
environments frequently disturbed by human activities (Sol et al.2014b). Adding the interaction between phylogenetic distance and degree
of habitat alteration improves the fit of previous models of invasion
success (Table S1 ). When considering this interaction, we find
support for the preadaptation hypothesis, with a negative relationship
between invasion success and phylogenetic distance but only for
human-altered environments, such as urbanized habitats (Fig.
4 ). Importantly, this pattern is not confounded by species richness
(Tables S2-S3 ) because urbanized environments tend to contain
fewer species than the surrounding non-urbanized environments (Solet al. 2020b).
While our results support the pre-adaptation hypothesis, they are not
exempt of potential biases. An issue that may make the patterns
difficult to interpret is that the subset of species that have been
introduced and successfully established in regions outside their native
range is a non-random sample of the entire avian phylogeny, a
possibility well-documented in the literature (Duncan et al.2003). The clustering of introduced species within the avian phylogeny
should increase the probability that a native species randomly selected
from the avian phylogeny belongs to a different clade. This effect may
be further accentuated by the fact that introduced species often come
from distant regions. For example, if we compare the phylogenetic
distances of pairs of species randomly sampled within and across the
main bioregions involved as donors and recipients of invaders, we find
that by chance the average distances across bioregions are higher than
within regions for a same sample size (Fig 2D, E ). To better
interpret the results, we assessed to what extent phylogenetic patterns
reflect ecological differences.
The notion that phylogenetic patterns reflect ecological differences is
supported by two lines of evidence. First, we found that the main axes
of niche variation across all species—measured in terms of morphology,
dietary use and foraging behavior (see methods)— showed clear evidence
of phylogenetic effects (Fig. S1) , supporting the existence of
substantial niche conservatism. A Mantel test further confirmed that
phylogenetic distance co-varied with niche differentiation (P =
0.001), although the analysis also showed that it only accounted for
31% of variation in the niche. Second, similar to phylogenetic
distance, we found a negative relationship between niche distance and
invasion success measured in terms of abundance (Fig. 4; Table
S4 ). The relationship between invasion success and niche distance
appears to primarily occur in human-altered environments (Fig.
4K,L,O,P ).
Instead, we found a different pattern when we examined the probability
that the invader occurred in a community within a given region. In
communities occupying less human-altered areas, this probability tended
to increase with functional distance, suggesting that invaders prefer to
settle in communities that lack species with similar niches
(Fig. 4I-N, Table S5 ). The alternative that the pattern results
from extinction of close-relatives by the invader is less likely because
invaders rarely achieved higher densities in little disturbed
environments. Moreover, native species are expected to be more
competitive than invaders in these environments because they have had
more opportunities to adapt (Sax & Brown 2000; Sol et al.2012a).
The discrepancy between patterns may indicate that functional and
phylogenetic distances contain different information. Phylogenetic
distances among species reflect differences in the niche, but they also
contain important information on traits related to the ability of the
species to persist in novel environments (Fig. 5) . While niche
availability is arguably essential to proliferate in a new environment,
response traits like behavioral plasticity and a future returns life
history strategy can also be important in novel environments to buffer
individuals against the demographic consequences of maladaptation (Solet al. 2012b). As response traits are particularly relevant to
live in human-altered environments (Sol et al. 2014a), it might
be that phylogenetic distance better captures differences among species
that are relevant for the pre-adaptation hypothesis than for the
naturalization hypothesis. This finding further highlights the
importance of using functional traits to interpret phylogenetic
patterns. It also suggests that the accuracy of predictive models should
increase when including functional information, a possibility supported
by our data (Table S1 ).
Our comprehensive analysis of phylogenetic relatedness between invaders
and natives yielded no support for naturalization hypothesis. Previous
works suggest that the failure to support the hypothesis reflects flaws
in the analyses, like the adoption of inappropriate spatial scales or
the use of taxonomic instead of phylogenetic information (Thuilleret al. 2010; Li et al. 2015). However, we analyzed
well-surveyed communities within a phylogenetic framework, and
considered possible sampling artifacts and a number of confounds such as
the body size of the invader and the relative abundance of native close
relatives. We also considered the possibility that native competitors do
not exclude invaders but merely reduce their abundance. Despite all
these improvements, we failed to find evidence that nonindigenous
organisms are more successful in communities in which their close
relatives are absent. While the role of competition in invasions remains
debatable, our results fit better with growing evidence that, at least
in birds (Duncan et al. 2003; Sol et al. 2012a),
competition only plays a minor role in explaining invasion success.
However, our finding that the probability that the invader occurred in a
community increased with functional distance may suggest that invaders
tend to avoid natural communities where they find species with similar
niche requirements. While human-altered environments are novel for both
invaders and native species, in natural environments the opportunity for
adaptation is substantially higher for native species. These communities
should thus exert stronger biotic resistance, which may in part explain
why exotic species tend to avoid them (Lovell et al. 2021).
However, our analyses indicate that the signatures of these effects are
difficult to detect with phylogenetic relatedness.
Our analyses provide more credence for the pre-adaptation hypothesis,
showing that phylogenetic distance is a good surrogate for both niche
and functional response traits and that lower functional distances are
also associated with enhanced invasion success. This results aligns with
growing evidence showing that invasion success in birds critically
depends on the possession of appropriate adaptations to flourish in
human-altered communities, where biotic resistance has been reduced by
the extinction of specialized competitors (Sol et al. 2012b).
Because these adaptations are phylogenetically conserved (Sol et
al. 2014a, 2017a, 2020b), it follows that the existence of
phylogenetically close species in the communities can inform us on the
likelihood that an invader establishes itself and spread in a new
region. Our findings thus extend those of Redding et al. (Reddinget al. 2019) by showing that the presence of closely related
species in a region not only increases the probability of establishment
but also the abundance a species attains, a key metric of invasion
success and a factor determining the impact of exotic species. This
provides some of the clearest evidence to date that the presence of
close relatives enhances —rather than inhibits— biological
invasions. It remains to be shown whether this conclusion can be
extrapolated to organisms with less ability than birds to sample
habitats and select those that best match their phenotypes.
We therefore conclude that phylogenies can improve our ability to
accurately predict the likelihood that a species proliferates when
introduced to a new region. However, phylogenetic information is only
useful to make predictions when considering the environmental context in
which invasions take place, particularly the degree of human-related
disturbances. Moreover, phylogenetic information should be combined with
functional data to accurately predict invasiveness, as phylogenetic
distances are not always an accurate surrogate of ecological distances.
The rapid development of new statistical techniques to integrate
phylogenetic and phenotypic information (Penone et al. 2014)
provides new, largely unexplored opportunities to improve our ability to
predict and prevent the success and impact of biological invasions.