![]()
Part I.
Basic Concepts of Alien Invasion and Evolution
In this introductory series of chapters, we outline the basic issues of evolutionary biology of alien species and consider basic aspects of dispersal capabilities and genetic variability that are central to the study of evolutionary change by aliens.
In chapter 1, we begin our examination by reviewing the magnitude and economic impact of worldwide introduction of plants, animals, and microorganisms to new geographic regions. Patterns of rapid evolution associated with these introductions are then presented, and their general significance is described. The major evolutionary issues that will be examined in succeeding chapters are then outlined.
Chapter 2 begins our examination of specific evolutionary issues by considering the selective pressures that act on mechanisms of dispersal by species poised to invade new regions or exposed to the agents of long-distance transport that modern human technology has created. The adaptations and evolutionary responses that enable the individuals that reach new regions to become established and spread are also discussed.
In chapter 3, we consider the patterns of genetic variability that species bring with them to new regions. First, we review the most important techniques of assessing genetic variability in populations of species, both in their native source populations and in newly established alien populations. We then consider how the processes of introduction and establishment tend to influence the genetic structure of founder populations.
Finally, in chapter 4, we examine how analysis of the genetic composition of populations of alien species in their native regions and regions of introduction can reveal precise source regions and invasion routes. In addition, these analyses often are able to distinguish cryptic aliensāforms not previously recognized as alien or not clearly distinguished from each other in their morphology.
These introductory discussions prepare us to proceed to an examination of the processes by which evolutionary change and adaptation occur in alien species in their new homes.
![]()
1.
Alien Species and Accelerated Evolution
āA growing appreciation that organic evolution, like mountain building, is an ongoing rather than simply historical process has stimulated an infusion of evolutionary thinking into mainstream ecology. Foremost among the factors that have fostered this development are reports of remarkable adaptive evolution known to have taken place in recent decades. . . . ā
āCARROLL ET AL. (2001)
Potato late blight (Phytophthora infestans) is a fungal disease of the Irish potato (Solanum tuberosum) and its relatives. The potato itself was domesticated in the Andean region of South America, whereas the blight fungus is believed to be native to the Toluca Valley of Mexico.The potato was introduced to Europe in the 1500s, and became a major food plant in Ireland and many other countries. A strain of the blight fungus somehow reached western Europe in the mid-1840s, where, coupled with weather conditions favorable to its development, it decimated potato crops. In Ireland, the almost total loss of the potato crop led to famine, in which 1.5 million people died and many more were forced to emigrate. Closely related strains of the fungus have since invaded all major potato-growing areas of the world. In the twentieth century, these strains have been more or less controlled by a combination of resistant potato varieties, fungicidal treatments, and sanitation.
Prior to the 1980s, strains of the blight fungus affecting potato and tomato (Lycopersicon esculentum) crops were of a single mating type, which reproduced asexually and showed little genetic variability. This genetic uniformity contributed significantly to the success of disease control. In the early 1980s, however, resurgence of late blight disease began to occur in the Old World, and by the late 1980s and early 1990s, severe outbreaks of the disease also affected potato crops in Canada and the United States (Fry and Goodwin 1997). These outbreaks were traced to new strains of late blight fungus that apparently originated in Mexico. The new strains were much more virulent and were resistant to one of the primary fungicides previously used to control late blight. These strains have already caused production losses measured in millions of dollars in parts of the Pacific Northwest.
Even more serious is the evolutionary potential created by these new forms of the late blight fungus. The new strains belong to the complementary mating type of the earlier fungus, so their arrival now makes possible sexual reproduction and resulting genetic recombination. Sexual reproduction has already been confirmed in several locations (Goodwin et al. 1998). New fungal strains that appear to be the result of recombination between different mating types have also been found on tomatoes in North Carolina (Wangsomboondee et al. 2002). Thus, the stage has been set for the rapid evolution of new genetic races of a fungus that is known to affect two of the worldās most important crops, potatoes and tomatoes, both of which are members of a plant family containing a host of other cultivated plants.
The Economic and Ecological Impact of Alien Species
Invasive alien species are now recognized throughout the world as one of the most serious ecological and economic threats of the new millennium (Pimentel 2002). Alien plants are reducing the productivity of agricultural crops, pastures, and rangelands and are disrupting many natural terrestrial ecosystems. In addition, alien plants are choking waterways and altering the function of freshwater and marine ecosystems. Many of these plants are now legally designated as noxious weeds. Alien animals are also altering the biotic structure of land, freshwater, and marine ecosystems and are pushing many native species toward extinction. Introduced disease agents are infecting crops, livestock, fish and game animals, timber trees, and horticultural plants. Increasingly, introduced diseases and their vectors are posing new threats to human health as well. The worldwide total of species introduced to new geographical regions by human agency probably approaches half a million species (Pimentel et al. 2001).
The direct and indirect economic costs of these invaders are enormous. In the United States alone, alien plants, animals, and microbes are estimated to cause economic losses of $137.2 billion annually (Pimentel et al. 2000), with estimates for agricultural losses worldwide reaching $248 billion (Pimentel et al. 2001). An additional $4.2 billion loss occurs in the United States due to alien forest insects and pathogens. Additional direct losses result from damage by aliens to fisheries, navigation, and industry. Still other costs are incurred in fighting alien species that are endangering native plants and animals. Invasions of natural ecosystems by alien species are degrading their unique aesthetic and recreational values.
Invasions of alien species are certain to continue, in spite of increasing awareness and prevention efforts. Much of this invasion is likely to occur as a result of increasing international trade and travel (Ewel et al. 1999). For the period from 1920 to 1990, for example, Levine and DāAntonio (2003) examined the relationship between value of foreign imports to the United States and the numbers of alien mollusks, plant pathogens, and insects becoming established.The most conservative model predicted that between 2000 and 2020 some three species of mollusks, five species of plant pathogens, and 115 species of alien insects are likely to become established in the United States. Less conservative models gave numerical predictions more than tenfold greater. Increased internal trade and traffic, including exchanges of organisms mediated via the Internet (see, e.g., Kay and Hoyle 2001), also mean that the spread of alien species within the United States and other countries will be great.
Alien Species and Contemporary Evolution
These threats, however, are only the tip of an ecological and evolutionary iceberg (Palumbi 2001). The worldwide introduction of alien species is leading to rapid evolutionary change in both alien species and the native species with which they interact. Contemporary in the sense that they occur over tens to hundreds of generations rather than millions of generations, these patterns of evolution are the result of profound human influences on the natural world (Stockwell et al. 2003). The introduction of alien species is interacting with habitat destruction and degradation, overexploitation of plants and animals in natural ecosystems, and global climatic change to create an evolutionary revolution. Patterns of rapid evolution involve all groups of organisms and all patterns of organismal interaction: plant-herbivore, prey-predator, and host-pathogen systems (Thompson 1998; Gilbert 2002). Far from slowing evolutionary change, humans have accelerated evolutionary processes.
Despite the serious impacts of alien species, their dynamic evolutionary potential has received little recognition. In particular, systems of regulation and management of these species have failed to recognize this potential. Alien species are classified as beneficial, harmless, or harmful, based on an evaluation of a limited sample of individuals at a particular time, with the usual result that they are either permitted or prohibited in commerce. Little attention is given to the risk of evolutionary change by alien species once they become established in a new region.
As we shall see, all species, both native and alien, are at all times subject to evolutionary pressures that may maintain an evolutionary status quo or may lead to gradual or rapid change in genetic characteristics. Freed, in many cases, from the constraints of gene flow from their parent population and from biotic pressures of former enemies, alien species acquire exceptional evolutionary opportunities. Because populations of alien species have become established in new physical and biotic environments, however, they are subject to altered selection pressures that are likely to bring about rapid evolutionary change. In their new environment, alien species may encounter close relatives from which they had been isolated geographically. Hybridization with these relatives may enhance their evolutionary potential. Furthermore, those aliens that become abundant and highly invasive impose strong new evolutionary pressures on the natives with which they interact.
The example of late blight of potatoes is only one of many cases in which alien species pose threats to human interests through their evolutionary potential. Strong anthropogenic selection pressures imposed by pesticides, antibiotics, and environmental pollutants such as heavy metals have long been known to induce resistance in plants, animals, and microbes. Numerous plants have shown rapid evolution of resistance to heavy metals in spoil heaps associated with mining activity (Macnair 1987). Literally hundreds of plants, animals, and disease organisms, many of them alien to the regions involved, have evolved resistance to pesticides (see, e.g., National Academy of Science 1986). More than 100 plants now show resistance to herbicides, with more being recorded annually.
The potential for alien species in general to show rapid evolutionary responses to other pressures, however, has been appreciated only in the last quarter century. Numerous examples of such evolutionary responses are now available. A recent survey (Reznick and Ghalambor 2001), for example, documented 34 studies of rapid evolution in response to agents other than pesticides, antibiotics, or pollutant chemicals. Most of these studies involve evolutionary changes following the introduction of a species to an environment with novel characteristics or to a new location. Some 18 of these studies reflected rapid evolutionary changes by alien speciesāorganisms that had invaded or been introduced to new geographical areas.
The risks of unexpected evolutionary responses of alien species have been increased by the rapidly expanding technology of genetic engineering. This is particularly true for genes that confer tolerance by crop species and other ābeneficialā organisms to herbicides or other pesticides, or that confer systemic resistance to pests or diseases. The majority of these genetically transformed species possess close relatives that are cropland weeds or wild ancestral species with the potential to evolve weed races. The possibility of escape of such genes via rapid evolutionary change demands the utmost caution in their introduction to open agricultural systems.
Appreciation is also growing that evolutionary change occurs within a community context, with change in individual species both being influenced by many other species and having impacts on other aspects of the community and ecosystem. This appreciation has led some to propose community genetics as a new subfield of science (Neuhauser et al. 2003). Whether or not such a branch deserves formal recognition, the fact is that rapid evolutionary change involving alien species and the natives with which they interact is proceeding on a very complex and influential ecological stage.
Adaptation of Alien Species for Dispersal
Dispersal is a basic life history process for all organisms and one of central importance to alien species. All species possess a life history stageāspore, seed, egg, larva, or mature organismāthat is adapted in some way for transport by wind or water currents, attachment to animal carriers, or active locomotion to sites that may offer suitable habitat. Plants and animals adapted to ephemeral or disturbed habitats have long been known for their ability to disperse widely and colonize new, often isolated sites. During human evolution, such species have proven to be well adapted to the habitats created by human activity. Many have followed humans as they migrated to new areas and often refined their life history traits to take advantage of humans, both as creators of habitat and as agents of dispersal. Such species are preadapted to spreading rapidly once they have been introduced to a new geographical region.
Many species have taken advantage of wheeled vehicles, seagoing ships, and airplanes as agents of transport, enabling them to cross major geographical barriers. Many of these species, especially plants, have been carried deliberately to new regions (see, e.g., Mack and Erneberg 2002), but others have hitchhiked. Modern systems of travel and commerce have become strong agents of selection for altered modes of reproduction and dispersal.The intimate association of weeds and other pests with crops and domestic animals, for example, is favored not only by the care that humans give to these domesticated species, but also by the enhanced probability that weed and pest progeny will be transported to new world regions (Gould 1991). Natural selection is constantly acting to fine-tune adaptations for dispersal by natural and human agency (Dieckmann et al. 1999).
Adaptation of Alien Species to New Environments
Alien species show diverse patterns of evolutionary adaptability when they arrive in new geographical regions. Each has a particular pattern of genetic variability that influences its potential for evolutionary change. In some cases, variability may be very limited due to the small number of individuals in the founding population. Genetic drift in small initial populations may further reduce variability by genetic bottlenecking. The genetic composition of a new population may be a biased sample of variability in the source population, the so-called founder effect.Thus, evolutionary responses may be constrained by lack of variability in many cases.
On the other hand, many colonizers, especially those of early succe...
