As many studies on biological invasions lack crucial data on which species have been introduced but failed to establish, we took advantage of a comprehensive list of alien plant species that have been introduced to Southern Africa for cultivation. This list allowed us to account for introduction biases in our tests of Darwin’s naturalization conundrum along the different stages of the invasion process. Our results show that alien species distantly related to native species were more likely to be introduced for cultivation. Once introduced, however, those that are more closely related to native species were more likely to naturalize. On the other hand, among the naturalized species in the country of South Africa, the ones most distantly related to the natives were more likely to become invasive. Our results thus show that phylogenetic distance to the native flora has opposing effects on the transitions during the invasion process.
Humans have introduced thousands of plant species from their native regions into foreign lands. Although some of those introductions were accidental, most of them were intentional for cultivation purposes40,57−60. Moreover, it is likely that the species that have been introduced are not a random selection from the global flora but possess certain characteristics that make them of interest for cultivation25,55. This is also reflected in their phylogenetic distance to the native flora, as we found that introduction of alien species for cultivation in Southern Africa was positively associated with phylogenetic distance to the native flora (Fig. 2a; Fig. 3d, e, f; Table S1). This most likely indicates that non-native species with characteristics that are missing in the native flora were more likely to have been prospected for cultivation in Southern Africa. For example, the fact that Australian Eucalyptus species —which have no close relatives in Southern Africa— grow faster and produce better wood than most native Southern African trees, made them very attractive for cultivation in forestry plantations61. The same is true for the introduction of other woody species to South Africa, that were planted for desertification control and to reduce firewood shortage62. In other words, our results are in line with the idea that humans might preferentially introduce plant species with characteristics that could provide economic and social benefits or ecosystem services that are not provided by species of the native flora.
Once introduced, not all alien species manage to grow and reproduce outside of cultivation. We found that the naturalization success of species introduced for cultivation was negatively associated with phylogenetic distance to the native flora (Figs. 2b, 3g, h, i; Table S1). In other words, and in line with the pre-adaptation hypothesis, introduced species that have closely related, and likely ecologically similar, species in the native Southern African flora were more likely to naturalize. This pattern was even visible when we considered the naturalization of all species in the global flora that are not native to Southern Africa (Fig. 3a, b, c; Table S1), despite the biased introduction of species that are distantly related to the native flora. This suggests that even if there is no information on which alien species have been introduced and failed to establish, comparing the naturalized ones to the global flora, as done in previous studies e.g.29,53,54, provides some indication of the importance of phylogenetic distance.
Naturalization in a new range depends on several abiotic and biotic factors1. These factors can act as filters that determine which species can in principle grow in the region, but biotic interactions such as competition can also provide resistance against the ultimate establishment of those species. It has been shown that, at least at the local scale, environmental pre-adaptation and biotic resistance are both important for alien plant naturalization38,43,63. However, in line with our results, at large spatial scales, environmental filtering is usually the most decisive factor for naturalization success28,39,50. One potential explanation, the pre-adaptation hypothesis proposed by Darwin36, is that introduced species closely related to the native flora share features with those native species that allow for survival and reproduction in the new range. These shared characteristics make the alien species pre-adapted to the new environmental conditions. While it is likely that closely related species have stronger competitive impacts on each other64–67 but see68, at large scales, the pre-adaptation effect may overrule the drawback of stronger competition from close relatives32,41,69. In a study that used functional traits of alien and native flora, Divíšek, et al.21 found that the similarity of alien and native species facilitates naturalization, but not invasiveness. This agreement with our study, suggests that this pattern persists even without accounting for the phylogenetic signal of species traits.
While the naturalization of introduced alien plants in Southern Africa might have occurred at sites where closely related native species happened to be present, this is less likely the case for naturalized species that have become widespread and locally dominant (i.e. invasive). In order for a naturalized species to spread and become dominant, it will have to interact with increasing numbers of native species. Those interactions are expected to be less detrimental for the alien species if it is more dissimilar to the natives, as this will allow it to avoid strong competition and common enemies by occupying vacant niches69,70. In line with this idea, we found that all naturalized species and the subset of cultivated naturalized species in South Africa were more likely to be invasive if they have no close relatives in the native flora. This has also been shown for alien trees and shrubs in Southern Africa71. It should be noted, however, that in this final stage of the invasion process, the three phylogenetic indices provided slightly different results. While the best fitting model revealed a monotonic increase of the probability of being invasive with increasing PDMin, the other models revealed marginal non-linear U-shaped trends for PDMean and PDwMean. At high values of PDMean and PDwMean, invasiveness probability also increased with increasing distance values, as it did with PDMin, but also showed a slight increase in probability at very low values of PDMean and PDwMean (Fig. 4a, b; Table S2). This not only suggests that naturalized species are more likely to become invasive when they are phylogenetically distant from the native flora, but also that closely related species could benefit e.g. by sharing pollinators72, and that super-competitors among alien species can outcompete closely related native species73. It could also reflect that closely related species have weaker negative allelopathic effects on each other, as recently shown by Zhang, et al.74.
Although we used three different phylogenetic distance indices, they largely revealed the same patterns. This is not surprising given that the indices are correlated. Nevertheless, models that included PDMin had the best fit. This suggests that for successful transitions from one stage of the invasion process to the next one, the phylogenetic distance to the native species most closely related to the alien species is more important than the average distance to all native species, weighted or unweighted with regard to commonness32. In another study, however, Malecore, et al.43 found that models that used PDMin consistently had the worst fit. This apparent discrepancy may reflect the difference in spatial scale between both studies. In our large-scale study, the most closely related native species is more likely to indicate whether there is a suitable habitat for the species somewhere in Southern Africa than the average distance to all native species does. At a smaller spatial scale, such as in the local plant communities of Malecore, et al.43, the unweighted or weighted mean distance to all native species might be a better indicator of the overall suitability of the local site for the introduced species.
In conclusion, our results show that the direction of the effect of phylogenetic distance of alien plants to the native flora alternated along invasion stages in Southern Africa. While introduction success was positively associated with phylogenetic distance to the native flora, the opposite was true for subsequent naturalization success, but invasiveness was again positively associated with phylogenetic distance. For the latter, the association might be non-linear, at least for the PDMean and PDwMean indices, with a tendency that not just distantly related aliens are more invasive but also aliens that are very closely related to natives. Thus, accounting for the different invasion stages and considering multiple phylogenetic distance metrics provide more insights into Darwin’s naturalization conundrum. Finally, yet importantly, the two seemingly opposing hypotheses of Darwin need not be in conflict. Rather, the mechanisms underlying them act concurrently, and the one that dominates depends on the alien species’ stage along the invasion process.