A recent trend in invasion ecology relates the success of non-indigenous species (NIS) to reduced control by enemies such as pathogens, parasites and predators (i.e. the enemy release hypothesis, ERH). Despite the demonstrated importance of enemies to host population dynamics, studies of the ERH are split -biogeographical analyses primarily show a reduction in the diversity of enemies in the introduced range compared with the native range, while community studies imply that NIS are no less affected by enemies than native species in the invaded community. A broad review of the invasion literature implies at least eight non-exclusive explanations for this enigma. In addition, we argue that the ERH has often been accepted uncritically wherever (i) NIS often appear larger, more fecund, or somehow 'better' than either congeners in the introduced region, or conspecifics in the native range; and (ii) known enemies are conspicuously absent from the introduced range. However, all NIS, regardless of their abundance or impact, will lose natural enemies at a biogeographical scale. Given the complexity of processes that underlie biological invasions, we argue against a simple relationship between enemy 'release' and the vigour, abundance or impact of NIS. KeywordsEnemy inversion hypothesis, enemy of my enemy hypothesis, enemy release hypothesis, exotic species, increased susceptibility hypothesis, invasion success, non-indigenous species.
The use of simple terms to articulate ecological concepts can confuse ideological debates and undermine management efforts. This problem is particularly acute in studies of nonindigenous species, which alternatively have been called ‘exotic’, ‘introduced’, ‘invasive’ and ‘naturalised’, among others. Attempts to redefine commonly used terminology have proven difficult because authors are often partial to particular definitions. In an attempt to form a consensus on invasion terminology, we synthesize an invasional framework based on current models that break the invasion process into a series of consecutive, obligatory stages. Unlike previous efforts, we propose a neutral terminology based on this framework. This ‘stage‐based’ terminology can be used to supplement terms with ambiguous meanings (e.g. invasive, introduced, naturalized, weedy, etc.), and thereby improve clarity of future studies. This approach is based on the concept of ‘propagule pressure’ and has the additional benefit of identifying factors affecting the success of species at each stage. Under this framework, invasions can be more objectively understood as biogeographical, rather than taxonomic, phenomena; and author preferences in the use of existing terminology can be addressed. An example of this recommended protocol might be: ‘We examined distribution data to contrast the characteristics of invasive species (stages IVa and V) and noninvasive species (stages III and IVb)’.
Anthropogenic climate change has already altered the timing of major life-history transitions, such as the initiation of reproduction. Both phenotypic plasticity and adaptive evolution can underlie rapid phenological shifts in response to climate change, but their relative contributions are poorly understood. Here, we combine a continuous 38 year field survey with quantitative genetic field experiments to assess adaptation in the context of climate change. We focused on Boechera stricta (Brassicaeae), a mustard native to the US Rocky Mountains. Flowering phenology advanced significantly from 1973 to 2011, and was strongly associated with warmer temperatures and earlier snowmelt dates. Strong directional selection favoured earlier flowering in contemporary environments (2010 -2011). Climate change could drive this directional selection, and promote even earlier flowering as temperatures continue to increase. Our quantitative genetic analyses predict a response to selection of 0.2 to 0.5 days acceleration in flowering per generation, which could account for more than 20 per cent of the phenological change observed in the long-term dataset. However, the strength of directional selection and the predicted evolutionary response are likely much greater now than even 30 years ago because of rapidly changing climatic conditions. We predict that adaptation will likely be necessary for long-term in situ persistence in the context of climate change.
Adaptation to climate, evolving over contemporary time scales, could facilitate rapid range expansion across environmental gradients. Here, we examine local adaptation along a climatic gradient in the North American invasive plant Lythrum salicaria. We show that the evolution of earlier flowering is adaptive at the northern invasion front where it increases fitness as much as, or more than, the effects of enemy release and the evolution of increased competitive ability. However, early flowering decreases investment in vegetative growth, which reduces fitness by a factor of 3 in southern environments where the North American invasion commenced. Our results demonstrate that local adaptation can evolve quickly during range expansion, overcoming environmental constraints on propagule production.
Biological invasions are 'natural' experiments that can improve our understanding of contemporary evolution. We evaluate evidence for population differentiation, natural selection and adaptive evolution of invading plants and animals at two nested spatial scales: (i) among introduced populations (ii) between native and introduced genotypes. Evolution during invasion is frequently inferred, but rarely confirmed as adaptive. In common garden studies, quantitative trait differentiation is only marginally lower (~3.5%) among introduced relative to native populations, despite genetic bottlenecks and shorter timescales (i.e. millennia vs. decades). However, differentiation between genotypes from the native vs. introduced range is less clear and confounded by nonrandom geographic sampling; simulations suggest this causes a high false-positive discovery rate (>50%) in geographically structured populations. Selection differentials (¦s¦) are stronger in introduced than in native species, although selection gradients (¦β¦) are not, consistent with introduced species experiencing weaker genetic constraints. This could facilitate rapid adaptation, but evidence is limited. For example, rapid phenotypic evolution often manifests as geographical clines, but simulations demonstrate that nonadaptive trait clines can evolve frequently during colonization (~two-thirds of simulations). Additionally, QST-FST studies may often misrepresent the strength and form of natural selection acting during invasion. Instead, classic approaches in evolutionary ecology (e.g. selection analysis, reciprocal transplant, artificial selection) are necessary to determine the frequency of adaptive evolution during invasion and its influence on establishment, spread and impact of invasive species. These studies are rare but crucial for managing biological invasions in the context of global change.
Invasion ecology has been criticised for its lack of general principles. To explore this criticism, we conducted a meta-analysis that examined characteristics of invasiveness (i.e. the ability of species to establish in, spread to, or become abundant in novel communities) and invasibility (i.e. the susceptibility of habitats to the establishment or proliferation of invaders). There were few consistencies among invasiveness characteristics (3 of 13): established and abundant invaders generally occupy similar habitats as native species, while abundant species tend to be less affected by enemies; germination success and reproductive output were significantly positively associated with invasiveness when results from both stages (establishment/ spread and abundance/impact) were combined. Two of six invasibility characteristics were also significant: communities experiencing more disturbance and with higher resource availability sustained greater establishment and proliferation of invaders. We also found that even though 'propagule pressure' was considered in only $29% of studies, it was a significant predictor of both invasiveness and invasibility (55 of 64 total cases). Given that nonindigenous species are likely introduced non-randomly, we contend that 'propagule biases' may confound current paradigms in invasion ecology. Examples of patterns that could be confounded by propagule biases include characteristics of good invaders and susceptible habitats, release from enemies, evolution of 'invasiveness', and invasional meltdown. We conclude that propagule pressure should serve as the basis of a null model for studies of biological invasions when inferring process from patterns of invasion.
Common garden studies are increasingly used to identify differences in phenotypic traits between native and introduced genotypes, often ignoring sources of among-population variation within each range. We re-analyzed data from 32 common garden studies of 28 plant species that tested for rapid evolution associated with biological invasion. Our goals were: (i) to identify patterns of phenotypic trait variation among populations within native and introduced ranges, and (ii) to explore the consequences of this variation for how differences between the ranges are interpreted. We combined life history and physiologic traits into a single principal component (PCALL) and also compared subsets of traits related to size, reproduction, and defense (PCSIZE, PCREP, and PCDEF, respectively). On average, introduced populations exhibited increased growth and reproduction compared to native conspecifics when latitude was not included in statistical models. However, significant correlations between PC-scores and latitude were detected in both the native and introduced ranges, indicating population differentiation along latitudinal gradients. When latitude was explicitly incorporated into statistical models as a covariate, it reduced the magnitude and reversed the direction of the effect for PCALL and PCSIZE. These results indicate that unrecognized geographic clines in phenotypic traits can confound inferences about the causes of evolutionary change in invasive plants.
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