Ecol Res (2007) 22: 849–854 DOI 10.1007/s11284-007-0435-3
Evolution in biological invasion
S P E C I A L IS SU E
Takehito Yoshida Æ Koichi Goka Æ Fumiko Ishihama Michihiro Ishihara Æ Shin-ichi Kudo
Biological invasion as a natural experiment of the evolutionary processes: introduction of the special feature
Published online: 24 October 2007 Ó The Ecological Society of Japan 2007
Abstract Although biological invasion has a devastating impact on biodiversity, it also provides a valuable opportunity for natural experiments on evolutionary responses. Alien populations are often subject to strong natural selection when they are exposed to new abiotic and biotic conditions. Native populations can also undergo strong selection when interacting with introduced enemies and competitors. This special feature aims to highlight how evolutionary studies take advantage of biological invasion and, at the same time, emphasizes how studying evolutionary processes deepens our understanding of biological invasions. We hope this special feature stimulates more invasion studies taking evolutionary processes into account. Those studies should provide fundamental information essential for formulating effective measures in conserving native biodiversity, as well as valuable empirical tests for evolutionary theories. Keywords Biological invasion Æ Rapid evolution Æ Phenotypic plasticity Æ Hybridization
T. Yoshida (&) Department of General Systems Studies, University of Tokyo, Komaba, Meguro, Tokyo 153-8902, Japan E-mail:
[email protected] Tel.: +81-3-54546645 Fax: +81-3-54546998 K. Goka Æ F. Ishihama National Institute for Environmental Studies, Onogawa, Tsukuba, Ibaraki 305-8506, Japan M. Ishihara Department of Biological Science, Graduate School of Science, Osaka Prefecture University, Gakuen-cho, Naka-ku, Sakai, Osaka 599-8531, Japan S. Kudo Department of Biology, Naruto University of Education, Naruto, Tokushima 772-8502, Japan
Introduction Human-associated dispersal of organisms can occur over very long distance such as hundreds and thousands of kilometers, in contrast to natural range expansion that usually happens over a much shorter distance. After the long history of both deliberate and unintentional human-associated dispersal, geographic barriers that have separated biogeographic provinces are now almost broken down, being called as a new, greatly shrunken Pangaea by Rosenzwerg (2001). What will happen to organisms if they disperse over such long distance? Human-assisted dispersal is likely to put alien populations into different environments or ecological conditions from those they originate. Those populations then experience new physical and chemical conditions, and interact with a different set of organisms from those in the native range. This exposure to new abiotic and biotic conditions will have a large effect on the ecology of introduced populations. They may go extinct or otherwise establish a new population, and sometimes increase their abundance massively so as to become ‘‘invasive.’’ Also, the exposure to a new environment is what imposes strong selection pressure on introduced populations. Native species that happen to interact with newcomers would undergo new selection as well. This is why biological invasion is recognized to be a good opportunity for natural unintentional experiments of evolutionary processes. In original conditions where source populations inhabit, we would expect that they are adapted to the local conditions. When they are exposed to new, different conditions after human-assisted long dispersal, their phenotypic distribution is likely to mismatch with new fitness optima, which results in strong directional selection and driving evolutionary response of the introduced population. However, this intuitive expectation may not be true, and the response to selection can be more complicated in nature (e.g., Lee 2002; Stockwell et al. 2003); many factors such as lack of genetic variability, negative genetic correlation and gene
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flow can limit the evolutionary response of a trait concerned. Nevertheless, evolutionary responses at contemporary time scales have been observed for a variety of organisms and ecological situations (e.g., Endler 1986; Thompson 1998; Hendry and Kinnison 1999). Those ongoing evolutions have provided valuable empirical tests for evolutionary theories, although naturally occurring evolution would be rarely witnessed. Unless drastic environmental changes and the resultant strong selection pressure can be predicted, it seems difficult to plan research detecting evolutionary responses beforehand. For example, in the 30-year study of Darwin’s finches by Grant and Grant (2002), rapid evolutionary changes occurred only sporadically, and there were repeated phases of evolutionary stasis. If one studied this system only for a limited time window, evolutionary responses would have not been observed. On the other hand, biological invasion is often caused by deliberate introduction of alien species or significant efforts are provided to detect and monitor biological invasions. Thus, among reported examples of contemporary evolutions, there are many cases of evolutionary responses associated with biological invasions (Sakai et al. 2001; Cox 2004; Sax et al. 2005). Biological invasion is now widely recognized to cause one of the most devastating impacts on biodiversity in a variety of ecosystems. Invasive species often cause extinction or otherwise large reduction of native species’ abundances, and they also change even the whole ecosystems and landscapes in some cases (e.g., Mack et al. 2000; Sakai et al. 2001). Such intensive adverse effect on biodiversity is predicted to continue in the future with its increasing magnitude (Sala et al. 2000). Studying evolutionary responses must deepen our understanding of biological invasions and their impact on native communities, which potentially leads to planning effective measures in conserving native biodiversity. In this introductory paper, we briefly describe contributed papers to this special feature in Ecological Research and present a short review of evolutionary processes relevant to biological invasion.
Evolutionary responses of aliens and natives in biological invasion Ecologists have long thought that the time scale of evolutionary processes is much longer than that of ecological processes, and thus evolutionary responses can be rarely observed at a contemporary time scale. Accumulating studies reported both in this feature and elsewhere are challenging this view. Introduced populations often evolve rapidly (e.g., Sakai et al. 2001; Cox 2004; Sax et al. 2005). In this special feature, Gomi (2007) reported trait adaptations of the fall webworm that was introduced to Japan from North America. This insect had a bivoltine life cycle (two generations per year) when introduced,
while they shifted to trivoltine 30-year after introduction. He studied some life history traits related to this life cycle shift and suggested that this insect adapted its traits to local climate conditions in the long islands of Japan by showing clear latitude clines in the traits. Togashi and Jikumaru (2007) reviewed the pine wilt disease occurring in Japan that is caused by an invasive nematode species. They identified virulence and transmission as important traits of parasitic nematodes. By comparing different alien genotypes and indigenous avirulent species, they suggested that evolution within a host pine tree likely played an important role in raising virulence of the invasive nematode, although more studies are needed to elucidate why this alien nematode became so invasive. Kudoh et al. (2007) studied the temperature-dependent germination process as a key life history trait that allowed a European weed plant to widely spread its distribution in Japan. By comparing the trait between introduced Japanese and native European strains, they suggested that the adaptation of this germination trait occurred during the introduction process into Japan. As seen in the above-mentioned studies, evolutionary responses of introduced populations are often studied by examining divergence processes exhibited in introduced populations that locally adapted after introduction or found between introduced and source populations. Discriminating different populations and reconstruction of invasion history are crucial in such studies. Miura (2007) pointed out that recently developing molecular genetic tools are useful in those tasks, as well as in detecting ‘‘cryptic invasions’’ of morphologically indistinguishable species from native ones. Molecular analysis can also measure genetic variation of introduced populations, which is thought to be a key factor in understanding invasion processes as discussed below. Successful invasion by alien populations often results in dramatic changes in native communities, and native populations that happen to interact with aliens will be exposed to new selection pressures. Evolutionary responses of native species are thus expected to occur, although they have been overlooked until recently (Strauss et al. 2006). In this feature, Chiba (2007) documented morphological and ecological shifts of a native land snail caused by the introduction of an alien predator, the black rat, into a small oceanic island. By examining changes in the snail that occurred within 19 years, during which time the introduced predator increased their abundance, he found that the snail shifted habitat use, which likely caused shell morphology shifts in an indirect manner. Carroll (2007) also reported the evolution of native phytophagous insects in response to invaded host plants, as well as other published cases of evolution of natives in response to biological invasion. In his own study on phytophagous insects, he conducted cross-breeding experiments in order to analyze the genetic architecture underlying insect adaptations and found the importance of non-additive genetic variation in the insect evolution.
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The growing list of studies reporting evolutionary responses of aliens and natives in biological invasion, including those reported in this feature, tells us that rapid, contemporary evolution in biological invasion is not rare, but rather pervasive. Adaptations of aliens and natives may influence the success of biological invasion and its consequences in native communities if natural selection not only acts on the genetic frequency change in a population, but also affects population demography through fitness changes. Lee (2002) and Stockwell et al. (2003) predicted the importance of rapid evolution in the establishment and invasion success of introduced populations.
Phenotypic plasticity in biological invasion Introduced populations often show evolutionary responses during successful invasions as we see above, whereas they may also exhibit plastic responses to new abiotic and biotic environments. Because the strong selection pressure is expected in biological invasion, organisms may respond and change their phenotype plastically in addition to responding genetically. In this feature, Collyer et al. (2007) examined whether introduced fish populations exhibited evolutionary or plastic responses to a new, introduced environment. They compared morphology between 30-year-old and 1-year-old populations after introduction from the same source population and found that morphological divergence was greater in a 30-year-old population than in 1-year-old ones. Although rapid evolutionary response was suggested, 1-year-old populations also showed the similar, but less morphological changes that are attributed to phenotypic plasticity. Yonekura et al. (2007) reported that despite a genetic bottleneck experienced during the introduction from a single origin, bluegill sunfish showed polymorphisms in their diet and corresponding feeding morphology in a Japanese lake where they became invasive successfully. Whether this polymorphism resulted from rapid evolution or phenotypic plasticity remains unclear, although this trophic differentiation is likely to have facilitated their successful invasion. Invasion biologists have sometimes attributed successful invasion to phenotypic plasticity. Baker (1965) proposed the concept of a ‘‘general purpose genotype’’ to describe successful invasive weed plants in a wide range of different environments. Indeed, some studies have shown that phenotypic plasticity facilitated successful invasion (e.g., Parker et al. 2003; Richards et al. 2006). However, whether plasticity is commonly important in explaining invasion success remains unclear (Lee 2002). Moreover, the relative importance of plastic and evolutionary adaptation has been studied rarely (Sakai et al. 2001). Although a few recent studies have examined their relative importance (Parker et al. 2003; Dybdahl and Kane 2005), we have to wait for a general picture until more studies assess impacts of both plastic and evolutionary responses to invasion success.
In addition, phenotypic plasticity itself can also evolve (Weinig 2000; Agrawal 2001), and this may make the analysis of the relative importance more complicated.
Hybridization in biological invasion Hybridization between aliens and natives receives notable attention from invasion biologists. Hybridization and introgression are suggested to cause extinctions of native populations, especially when they are rare in abundance (Rhymer and Simberloff 1996; Ellstrand et al. 1999). Hybridization provides introduced populations a source of new genetic variation that is remarkably reduced when they are introduced from source populations (Ellstrand and Schierenbeck 2000; Mooney and Cleland 2001), which likely results in successful invasion because increased genetic variation allows fast adaptation to a new environment. Polyploidy is another characteristic possibly produced by hybridization that leads to successful invasion. Polyploid hybrids tend to show higher growth rates than diploid parents because polyploids have some attributes including higher levels of heterozygosity and reduced inbreeding depression (Soltis and Soltis 2000). In this special feature, Bailey et al. (2007) discussed the role of polyploidy and hybridization in successful invasion of a weed plant that was introduced from Asia to Europe. Introduced weeds first spread their distribution by their vigorous vegetative growth, and then they formed hybrids between each other, which increased genetic variability of this weed plant. The increased genetic variation seems responsible for their invasion success. Among other cases where hybridization is attributed to successful invasion, hybridization between Japanese and European dandelions has been reported in Japan (Morita et al. 1990; Shibaike et al. 2002). Various types of hybrids between native and alien dandelions have been spreading their distributions, which may be explained by competitive dominance of hybrids resulting from some ecological characteristics such as high survivorship in early life stage (Hoya et al. 2004). Although introgressive hybridization has been suggested as an important process in biological invasion, the only limited number of risk assessment models of invasion has taken hybridization into consideration. Tanaka (2007) reviewed theoretical and empirical studies on introgressive hybridization. He stresses that explicit inclusion of population genetic mechanisms of hybridization is important in developing a risk assessment model that predicts genetic extinction of native populations due to hybridization.
Relative importance of ecology and evolution Individuals within a population are not equal to each other, and they frequently show remarkable genetic
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variations in various traits including morphology, physiology, behavior and life history. Despite the recognition of such genetic variations within populations and earlier theoretical studies suggesting the importance of genetic variation in population dynamics, most population and community ecologists have assumed that organisms have a fixed set of traits, and trait variations do not change ecological interactions and thus are irrelevant to population and community dynamics (e.g., Thompson 1998; Saccheri and Hanski 2006). This prevailing view has been challenged by recent empirical studies. These studies showed that trait genetic variation and its fluctuation can indeed influence population and community dynamics (e.g., Sinervo et al. 2000; Yoshida et al. 2003). The influence of trait variation on population and community ecology through alternation of ecological interaction would be more common than most ecologists assume. However, we do not know the definite role of evolution yet, because too few studies have examined the relative importance of ecology and evolution in biological invasions (Lambrinos 2004). The actual degree of evolutionary effects on biological invasions remains to be studied. For example, Takamura (2007) reviewed various factors resulting in the invasion success of largemouth bass from North America to Japan. Ecological factors such as refuge availability for prey were suggested to determine the predatory impacts of largemouth bass on native prey fish, while other evolutionary factors such as hybridization between introduced bass populations from different sources seem relevant to invasion success. However, the relative importance of ecology and evolution has not been evaluated yet. Kinnison et al. (2007) discussed several issues that limit the integration of contemporary evolution into Fig. 1 Sequence of biological invasion and example evolutionary responses that would influence whether and how fast each event proceeds to the next
conservation biology. They emphasized that the recognition of these issues by conservation biologists will make their practices more effective. The issues they discussed include the perception of similar timescales of evolutionary and ecological processes, contemporary evolution as an ecological process, linking traits with fitness of a population of interest, and influence of dispersal and gene flow on evolution. They also pointed out that conservation practices such as captive propagation and refuge population would need reconsideration with respect to contemporary evolution.
Conclusions Biological invasion is an ecological process where alien populations colonize a new habitat, establish their populations and influence native populations by increasing their abundance. Thus, it has many facets of ecological interactions among aliens, natives and colonized environment that sometimes exhibit strong selection pressures on alien and native populations (Fig. 1). Evolutionary responses to such strong selection pressure have been observed in studies reported in this feature and elsewhere. Thus, biological invasion provides a good opportunity of a natural experiment for evolutionary studies. This is, however, not to say that biological invasion can be justified, rather studying evolutionary processes in biological invasion should deepen our understanding of this ecological phenomenon. Biological invasion can also offer a pilot study of adaptation to global climate change. Predicted climate change is expected to alter distribution of many organisms, whereas populations especially located at the edge
invasion sequence
example evolutionary response
evolution of dispersal ability adaptation to human transport
adaptation to new environment increase genetic variation (e.g. hybridization)
evolution of competitive ability adaptation to new resources evolution of fitness
evolution of natives coevolution of aliens & natives
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of distribution ranges would be exposed to selection pressure due to changed environment. Adaptation to a new environment may influence how organisms alter their distributions in response to global climate change (e.g., Geber and Dawson 1993; Hampe and Petit 2005). In biological invasion, introduced populations are often exposed to new environments they have never experienced before. Thus, studying adaptation in biological invasion provides another type of natural experiment to study how unprecedented climate change influences organisms. Although we have a growing list of examples reporting evolutionary responses of aliens and natives, it is still unclear whether such evolution changes the success of biological invasion and its consequences on native communities. As Kinnison et al. (2007) pointed out, linking trait evolution with fitness evolution is the next pivotal task in understanding the effect of evolution on biological invasion. If evolution changes the fitness of aliens and natives, ecological interactions involved in those populations will become variable and different from what we expect based on ecological characteristics they show in their native or unaffected ranges. Because of the recently recognized possibility that evolution can indeed alter population dynamics (Yoshida et al. 2003; Hairston et al. 2005), we should not neglect the evolutionary effects when we try to understand biological invasions and their impacts on native communities. Acknowledgments This special feature is edited based on a symposium held at the annual meeting of the Ecological Society of Japan (ESJ) in Niigata city on 25 March 2005, together with contributions from other ecologists who study evolutionary processes in biological invasions. We thank all contributors to this feature. We also thank the ESJ for supporting the symposium and Yoh Iwasa, the editor-in-chief, for giving us an opportunity to publish this special feature.
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