Natives Adapting to Invasive Species: Ecology, Genes, and the Sustainability of Conservation
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Ecol Res (2007) 22: 892–901 DOI 10.1007/s11284-007-0352-5 SPECIAL ISSUE Evolution in biological invasion Scott P. Carroll Natives adapting to invasive species: ecology, genes, and the sustainability of conservation Received: 6 October 2006 / Accepted: 10 January 2007 / Published online: 9 March 2007 Ó The Ecological Society of Japan 2007 Abstract Contemporary anthropogenic evolution is Japanese honeysuckle (Lonicera japonica) was intro- common. Biological invasions are an especially dynamic duced into the eastern United States for horticulture form of novel selection. This paper considers how native 200 years ago and began naturalizing widely by the early species evolve in response to biological invasions and the 1900s. With the introduction of other East Asian hon- potential consequences of such evolution. Among eysuckles that similarly became abundant environmental numerous recent cases, the most widely reported in- weeds (Hartman and McCarthy 2004), hybrid swarms of stances are of phytophagous insects shifting onto complex parentage developed (Rehder 1947). In 1997, introduced host plants. For example, our studies show native North American tephritid fruitflies were discov- that in North America and Australia, soapberry bugs ered infesting wild, hybrid East Asian honeysuckles in evolved substantially after colonizing introduced hosts. Pennsylvania (Schwarz et al. 2005). In their native ran- Such cases permit close estimation of evolution’s direc- ges, the introduced honeysuckle taxa are hosts for Asian tion and rate, and we have used cross-rearing studies of Rhagoletis, but no infestation of introduced or native derived and ancestral-type populations to measure Lonicera by Rhagoletis has been previously reported changes in reaction norms and performance tradeoffs. from North America. Different fitness traits have followed very different paths Genetic analyses of the flies newly parasitizing Loni- in evolving to their current phenotypic values. Our cera fruit showed them to be a monophyletic group hybridization studies show that the genetic architecture overlapping with the invaders’ geographic distribution. of these adaptations involves a surprising degree of non- Yet they were not identifiable to a known Rhagoletis additive variation (epistasis, dominance). The impor- taxon; instead, they have a unique allelic mixture formed tance of non-additive genetic variation in rapid evolu- through the hybridization of two native fly taxa: R. tion will be clarified as more studies take advantage of mendax, which uses native blueberry fruit (Arctostaph- similar situations. As appreciation grows for the deep ylos), and R. zephyria, which uses native snowberry fruit contemporary interplay of evolution and ecology, de- (Symphoricarpos). Due to its hybrid origin, the new bate about qualitative terms describing evolution’s rate taxon differs genetically and appears to be reproduc- will become less relevant. From a conservation stand- tively isolated from its parental taxa. The Lonicera fly is point, contemporary evolution in native species presents regarded as a new species (Schwarz et al. 2005) that challenges for ecologically appropriate and sustainable ‘‘suddenly’’ evolved as a host specialist in response to management. Evolving natives and invaders may rec- swift ecological changes rendered by Asia-native plants onfigure contemporary and future communities. Adap- invading North America. tive evolution may also enhance native communities’ The rapid origin of a new species in response to a capacity to control invasive populations. nonnative weed reveals the biological complexity of invasion issues and the implications of evolutionary re- Keywords Rapid evolution Æ Soapberry bug Æ sponses to global change. The major factors destroying Biological invasion Æ Conservation Æ Genetics Earth’s biodiversity are describable in simple terms: destruction comes from eliminating and converting habitats that kills individuals and prevents reproduction. S. P. Carroll Poisoning, over-harvesting, species introductions and Department of Entomology and Center for Population Biology, climate change further alter habitats, disintegrate natu- University of California, Davis, CA 95616, USA ral communities, alter niches and reduce carrying E-mail: [email protected] capacity (e.g., Cox 2004; Diamond 1989). When re- Tel.: +1-530-2976080 Fax: +1-530-2976080 sources change in form, distribution and abundance, 893 they create new niches, affect competition, eliminate invasive species may alter native communities and how enemies and recast the landscape for surviving taxa. quickly they may do so. As chronicled perturbations, These ecological changes raise the possibility that invasion events offer increasingly commonplace oppor- adaptive evolution, emerging from the demographic tunities to test ideas about how communities assemble chaos suffered by ‘refugee taxa,’ will prove to be fore- (Strauss et al. 2006a). As researchers exploit more of most in altering the form and structure of species and these opportunities, we will better understand how communities in the coming years, decades and millennia. invasive species integrate into new communities. A chief result of efforts to secure sanctuary for species This paper examines how native species may evolve in and biota will be to provide raw material for such evo- response to biological invasions and the potential con- lution. Accordingly, a principal challenge of conserva- sequences of such evolution. Evolutionary changes in tion biology is to predict and manage the structure of both native and exotic taxa may determine how com- communities that have unprecedented assemblages of munities reconfigure following invasion (Cox 2004; juxtaposed, and rapidly evolving, remnant species Lambrinos 2004; Strauss et al. 2006a; Vermeij 1996; (Carroll 2007; Strauss et al. 2006a). Yoshida et al. 2003). This paper also reviews work The human-influenced geographic shuffling of organ- about rapid evolution in an insect seed predator in re- isms is probably the most biologically dynamic of anthro- sponse to introduced plants, describes the ecological and pogenic ‘global change’ phenomena. Nonindigenous genetic bases for its ongoing adaptive evolution and (a.k.a. ‘nonnative’ or ‘introduced’) species are popula- evaluates ecological and conservation consequences of tions of organisms not native to a particular habitat. If such fundamental change in species. established populations of a nonnative species grow and spread due to successful reproduction and recruitment of subsequent generations into the breeding population, Phylogeny and ecology in invasions of native communities that species may become prominent in the native biota, or ‘invasive’ (Parker et al. 1999; Richardson et al. 2000). Colonists from biologically distant locales that survive Invasive species may become numerically and ecologi- and reproduce in a new habitat will form a variety of cally dominant to native populations (Crooks 2002; relationships with natives. How those relationships de- Davis and Thompson 2000). velop depends on a variety of factors. The colonists’ Disturbed habitats may lose constituent species and degree of pre-adaptation may strongly influence how are more susceptible to nonindigenous taxa (e.g., Davis quickly their population grows and the form and et al. 2000; Elton 1958; Rejmanek et al. 2004). Nonin- strength of their interactions with natives. Pre-adapta- digenous organisms may become established in dis- tion may mean that a colonist can readily find resources, turbed habitats by accessing resources left unused escape from enemies or avoid abiotic perils. For exam- because resident taxa are reduced (Fargione and Tilman ple, Strauss et al. (2006b) found that in California, 2005; Levine et al. 2004), or because they are better grasses with few close relatives in the native flora were adapted to disturbed habitats than are residents (e.g., more likely to invade than were those with many close Burke and Grime 1996; Strauss et al. 2006b). Whether in relatives, implying that resources were more available disturbed habitats or not, nonindigenous species may, (or risks lower) for genetically distant colonists. The during introduction, escape natural enemies in ways that relatively more novel genotype-by-environment interac- give them a competitive advantage over residents regu- tions represented by new genera (rather than species in a lated by activity at higher tropic levels (e.g., Colautti genus already present) colonizing a habitat may repre- et al. 2004; Joshi and Vrieling 2005; Stastny et al. 2005). sent an instantaneous ‘‘niche-creation’’ process. Thus, as an introduced species transitions into a com- In such cases, where colonization succeeds due to low munity, the ecological circumstance of the invasion, as levels of competition with natives, impacts on native well as the invading population’s genetic history, may communities may (at least initially) be slight. Colonist influence niche opportunities available to the newcom- populations may then grow until interspecific competi- ers. tion for one or more resources becomes important. To Invasive species necessarily exist within biotic com- the extent that colonists have certain advantages over munities, and thus play many parts in ecological webs. natives (e.g., enemy-free space), they may out-compete They can be predators, pathogens, parasites, competi- them and become deleteriously invasive. tors, mutualists or hosts (e.g., Mitchell et al. 2006). The hypothesis that invaders may prosper due to Certain prominent