The rise in human transportation has lead to a substantial increase in species movements out of their native geographic ranges, ultimately resulting in biotic homogenization of ecosystems world-wide and dramatic changes in ecosystem functioning (Mooney & Hobbs, 2000; Thuiller, 2007). Understanding and predicting the spread and impact of invasive species thus have become central research objectives in fundamental and applied ecology (Nentwig, 2007; Walther et al., 2009). In particular, invasion ecology has focussed on two questions: (1) which species traits make introduced species more likely to become invaders (Rejmánek, 1995; Thuiller et al., 2006; Pyšek & Richardson, 2007)? and (2) why are some natural communities more prone to invasion than others (Davis et al., 2000; Levine et al., 2004; Tilman, 2004; Richardson et al., 2005)?
Recently, there has been a renewed interest in long-standing hypotheses that merge the two questions by focusing on the phylogenetic relatedness between potential invaders and recipient communities (Fig. 1). Based on an original observation of De Candolle (1855), Darwin (Darwin, 1859), in The origin of species, hypothesized that immigrant species are more likely to naturalize when they belong to genera with no native species in the region. This hypothesis, termed ‘Darwin’s naturalization hypothesis’ (Rejmánek, 1996), states that introduced species that are phylogenetically unrelated to local communities should be more successful because they can exploit unfilled ecological niches in native communities (Fig. 1). It implies niche differentiation and niche gap-filling from invaders to be the main drivers of invasion success. However, Darwin also recognized that immigrant species from native genera might have a better chance to naturalize because they share similar pre-adaptations to local environmental conditions with allied species. Following this line of argument, an increase in the phylogenetic relatedness between an introduced species and its recipient community increases its probability of invasion (Fig. 1). This implies that related species have similar environmental requirements and/or benefit from mutualistic or facilitative interspecific interactions because of their shared evolutionary history (Bruno et al., 2003; Wiens & Graham, 2005). These two seemingly contradicting hypotheses, i.e. that introduced species are more likely to naturalize when they are phylogenetically similar versus dissimilar to the native community, have both been originally proposed by Darwin (1859) and are therefore encapsulated under the term ‘Darwin’s naturalization conundrum’ (Diez et al., 2008). Both hypotheses make testable predictions: if species with non-overlapping niches in time or space are more likely to co-exist (Chase & Leibold, 2003), and if species niches have been conserved during evolutionary history, then successful invaders should exhibit a particular phylogenetic position relative to native communities.
A number of recent studies have tested these predictions with empirical data. They have in common that they have treated the two hypotheses as mutually exclusive (with the exception of Diez et al., 2008 and Procheşet al., 2008). However, few, if any, general patterns emerged (Table 1). Of course, the discrepancy between studies may partly be explained by different biological systems and environmental settings that may influence the relative importance of environmental filtering versus biotic interactions in driving community assembly. However, we argue that much of the inconsistency is ostensible and arises from discrepancies in the applied conceptual frameworks and analytical approaches. To our understanding, the main three points that have obscured a general understanding of community invasibility by the mean of species dissimilarity are a matter of spatial and phylogenetic scale, a matter of metric and null expectations and a matter of quantification of niche (dis)similarity. The application of a standard framework across different biological systems should ultimately allow us to assess whether Darwin’s naturalization hypotheses can explain current patterns of biological invasions.
|Reference||Taxa||Spatial scale/spatial grain||Phylogenetic level||Statistic model (test)||Species pool||Additional information||Conclusion|
|Rejmánek (1996)||Plants (Gramineae, Compositae)||California/California||Genus||Number of naturalized species vs. species pool against number of species in European only vs. shared genera (contingency table, Chi-square test)||‘Available’ species from area of origin (Europe)||+|
|Daehler (2001)||Plants (Angiosperms)||Hawai/Hawai||Family (pooling multiple genera)||Probability that naturalized species belongs to native genera (expectation under binomial distribution)||1. Global species of families with naturalized species 2. All naturalized (early vs. later naturalized) 3. All accidentally naturalized (early vs. later naturalized)||1., 2. and 3.|
|Duncan & Williams (2002)||Plants (Angiosperms, Gymnosperms)||New Zealand/New Zealand||Genus||Naturalization rate (number of naturalized species as a proportion of pool) ∼ ‘genus having at least one native species (fixed effect) + family (random effect) (GLMM)||Genera containing introduced species||−|
|Ricciardi & Atkinson (2004)†||Aquatic systems (fishes, invertebrate, algae and vascular plants)||Global/sites||Genus||Number of high-impact invaders vs. number of low-impact invaders against number of invaders in genera shared vs. unshared with natives (meta-analysis of region-specific contingency tables, Fisher Exact tests)||All invaders||+|
|Lambdon & Hulme (2006)||Plants||Islands of the Mediterranean Basin/regional, local and habitat||Genus, family, order, subclass||Naturalization status (0/1) ∼ presence of congeneric + species variables + island variables (GLM)||Common invaders||Species characteristics, island characteristics, habitat characteristics, introduction frequency||0‡|
|Ricciardi & Mottiar (2006)||Fishes||Global/sites||Genus||Number of successful invaders vs. number of failed invaders against number of invaders in genera shared vs. unshared with natives (meta-analysis of region-specific contingency tables, Fisher Exact tests)||All introduced species||0|
|Strauss et al. (2006)†||Plants (Gramineae)||California/California||Phylogenetic supertree||Phylogenetic distance (mean distance to natives, distance to nearest native relative) ∼ pest vs. non-pest invaders (t-test)||All naturalized||Area of origin||+|
|Diez et al. (2008)||Plants||Aukland region/Aukland region, habitat||Genus||1. Probability of naturalization ∼ number of native congenerics + abundance of native congenerics 2. Exotic abundance ∼ number of native congenerics (region) + abundance of native congenerics (region) 3. Exotic abundance ∼ number of native congenerics (habitat) + abundance of native congenerics (habitat) (hierarchical Bayesian framework)||All introduced species||Habitat characteristics, stages of invasion (naturalization and spread), naturalization period||1. |
+ (abund.) 2.
− (abund.) 3.
|Diez et al. (2009)||Plants||Australia and New Zealand/Australia and New Zealand, Australia vs. New Zealand||Family, genus||Probability of naturalization ∼ presence of native congenerics + genus + climatic origin + family (random effect) (hierarchical Bayesian framework)||All introduced species||Climatic origin||−*|