Revisiting Darwin's conundrum reveals a twist on the relationship between phylogenetic distance and invasibility

Abstract

A key goal of invasion biology is to identify the factors that favor species invasions. One potential indicator of invasiveness is the phylogenetic distance between a nonnative species and species in the recipient community. However, predicting invasiveness using phylogenetic information relies on an untested assumption: that both biotic resistance and facilitation weaken with increasing phylogenetic distance. We test the validity of this key assumption using a mathematical model in which a novel species is introduced into communities with varying ecological and phylogenetic relationships. Contrary to what is generally assumed, we find that biotic resistance and facilitation can either weaken or intensify with phylogenetic distance, depending on the mode of interspecific interactions (phenotype matching or phenotype differences) and the resulting evolutionary trajectory of the recipient community. Thus, we demonstrate that considering the mechanisms that drive phenotypic divergence between native and nonnative species can provide critical insight into the relationship between phylogenetic distance and invasibility.nvasive species are a major cause of concern due to their large ecological, social, and economic consequences (1-3). In principle, future invasions could be avoided by preventing introductions of potential invaders into susceptible communities. Thus, research has focused on identifying the characteristics that predispose species to becoming invasive (4-7) and the properties that make communities susceptible to invasion (8, 9). Although generalities have been elusive, one approach that has recently been gaining interest is using phylogenetic distance (time since cladogenesis) between nonnative species and species in the recipient community as an indicator of invasion potential.Darwin was the first to suggest that the probability of establishment by introduced species depends on their relatedness to native species (10). However, as Darwin noted, the ecological similarity of related species can have opposing effects on their potential for coexistence ("Darwin's naturalization conundrum"). On the one hand, establishment in regions with close relatives should be facilitated by favorable abiotic conditions and the presence of suitable prey, hosts, and mutualists (Fig. 1A). On the other hand, establishment in these regions should be inhibited by competition with the relatives themselves and exploitation by shared natural enemies (Fig. 1B). Citing observations by Alphonse de Candolle and Asa Gray that naturalized species are more frequently from nonnative genera, Darwin concluded that competition was the dominant factor and relatedness to native species should reduce establishment success ("Darwin's naturalization hypothesis").However, recent studies using statistical models, molecular phylogenetics, and experimental community assembly have revealed that the correlation between relatedness and establishment probability can be positive, negative, or zero (Table 1). These findings call into question the paramoun...

Evaluating Darwin’s Naturalization Hypothesis in Experimental Plant Assemblages: Phylogenetic Relationships Do Not Determine Colonization Success

“…A hypothesis opposed to DNH is related with preadaptation [29], [42]–[43], which proposes that phylogenetic closeness promotes the colonization process through facilitation among related taxa [41]–[42], [44]–[45]. Our results do not support this hypothesis, because colonization by Lactuca did not show a positive association with the phylogenetic relatedness of the assemblages.…”

“…Our results suggest that under the spatial scale used there was a null effect of the phylogenetic distance on colonization success and the invasion’s contingent conditions such as the current properties of resident assemblage, and the intrinsic properties of invaders would be more relevant in determining colonization success than factors associated with phylogenetic relatedness, as has been discussed by other authors [10], [41], [43], [46], [47]. This does not mean that phylogenetic distance between invader and resident assemblage does not affect the colonization process.…”

“…A recent study [21] evaluated the change in the intensity of the interactions between vascular plant species along a phylogenetic gradient (with MNND distances ranging between 0 my and 81 my). Although these experiments were made between pairs of species and not in communities, the support of DNH was only partial because the evolutionary closeness not only allowed greater inhibitory interaction intensity (such as competition), but it also increased the intensity of facilitating interactions, which have an effect that is the opposite of that expected by DNH [10], [43]. From the community viewpoint it would be extremely important to quantify the combined effect of the inhibitory and facilitative interactions on the success of colonization, and how this balance is expressed along the colonizer-community relatedness gradient.…”

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.…”

Explaining invasion success of non-native trees in Southern Africa

“…Secondly, successful invaders might be expected to be more closely related to the native species pool because they share traits that pre-adapt them to the new environmental conditions in which they find themselves. Tests of Darwin's naturalization hypotheses have been mixed, and opposing predictions and mechanisms have been proposed (see Table 1 in Jones, Nuismer & Gomulkiewicz 2013). For example, there has been both documented evidence for increased susceptibility to attack by natural enemies (Hill & Kotanen 2009; Ness, Rollinson & Whitney 2011) and increased mutualisms (Richardson et al 2000b) among non-natives closely related to the native species pool.…”