Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions

Invasive species are predicted to suffer from reductions in genetic diversity during founding events, reducing adaptive potential. Integrating evidence from two literature reviews and two case studies, we address the following questions: How much genetic diversity is lost in invasions? Do multiple introductions ameliorate this loss? Is there evidence for loss of diversity in quantitative traits? Do invaders that have experienced strong bottlenecks show adaptive evolution? How do multiple introductions influence adaptation on a landscape scale? We reviewed studies of 80 species of animals, plants, and fungi that quantified nuclear molecular diversity within introduced and source populations. Overall, there were significant losses of both allelic richness and heterozygosity in introduced populations, and large gains in diversity were rare. Evidence for multiple introductions was associated with increased diversity, and allelic variation appeared to increase over long timescales (~100 years), suggesting a role for gene flow in augmenting diversity over the long‐term. We then reviewed the literature on quantitative trait diversity and found that broad‐sense variation rarely declines in introductions, but direct comparisons of additive variance were lacking. Our studies of Hypericum canariense invasions illustrate how populations with diminished diversity may still evolve rapidly. Given the prevalence of genetic bottlenecks in successful invading populations and the potential for adaptive evolution in quantitative traits, we suggest that the disadvantages associated with founding events may have been overstated. However, our work on the successful invader Verbascum thapsus illustrates how multiple introductions may take time to commingle, instead persisting as a ‘mosaic of maladaptation’ where traits are not distributed in a pattern consistent with adaptation. We conclude that management limiting gene flow among introduced populations may reduce adaptive potential but is unlikely to prevent expansion or the evolution of novel invasive behaviour.     

Adaptive Release of Natural Enemies in a Pest-Natural Enemy System with Pesticide Resistance

Integrated pest management options such as combining chemical and biological control are optimal for combating pesticide resistance, but pose questions if a pest is to be controlled to extinction. These questions include (i) what is the relationship between the evolution of pesticide resistance and the number of natural enemies released? (ii) How does the cumulative number of natural enemies dying affect the number of natural enemies to be released? To address these questions, we developed two novel pest-natural enemy interaction models incorporating the evolution of pesticide resistance. We investigated the number of natural enemies to be released when threshold conditions for the extinction of the pest population in two different control tactics are reached. Our results show that the number of natural enemies to be released to ensure pest eradication in the presence of increasing pesticide resistance can be determined analytically and depends on the cumulative number of dead natural enemies before the next scheduled release time.     

The genetic architecture of parallel armor plate reduction in threespine sticklebacks

How many genetic changes control the evolution of new traits in natural populations? Are the same genetic changes seen in cases of parallel evolution? Despite long-standing interest in these questions, they have been difficult to address, particularly in vertebrates. We have analyzed the genetic basis of natural variation in three different aspects of the skeletal armor of threespine sticklebacks (Gasterosteus aculeatus): the pattern, number, and size of the bony lateral plates. A few chromosomal regions can account for variation in all three aspects of the lateral plates, with one major locus contributing to most of the variation in lateral plate pattern and number. Genetic mapping and allelic complementation experiments show that the same major locus is responsible for the parallel evolution of armor plate reduction in two widely separated populations. These results suggest that a small number of genetic changes can produce major skeletal alterations in natural populations and that the same major locus is used repeatedly when similar traits evolve in different locations.     

Analysis of importations for biological control of insect pests and weeds in New Zealand

Importations of biological control agents for insect pests and weeds in New Zealand are summarized and factors contributing to the relative success of the programmes are examined. The establishment rate of 30.9% is similar to that achieved worldwide, but is significantly lower than the rate achieved in the island habitat of Hawaii. The pioneering role of New Zealand in biological control is shown by the high proportion of programmes first attempted in this country. Although this novelty has not reduced the establishment rate, introductions against endemic species have not succeeded. Size of release was not a dominant feature in the establishment of agents. Complete or substantial success is recorded for 17 of the 70 target pests, with a relatively high success rate in forestry programmes. Examples of the influence of climate matching and competitive exclusion are also discussed. Changing practices and attitudes to the introduction of biological control agents are documented to show the increasing emphasis on specialists. No adverse effects of introductions are reported. The challenge to practitioners and regulators is to develop systems to evaluate conflicts of interest and develop workable mechanisms to determine which biological control agents are suitable for release.     

Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective

Ticks had to adapt to an existing and complex vertebrate hemostatic system from being free-living scavengers. A large array of anti-hemostatic mechanisms evolved during this process and includes blood coagulation as well as platelet aggregation inhibitors. Several questions regarding tick evolution exist. What was the nature of the ancestral tick? When did ticks evolve blood-feeding capabilities? How did these capabilities evolve? Did host specificity influence the adaptation of ticks to a blood-feeding environment? What are the implications of tick evolution for future research into tick biology and vaccine development? We investigate these questions in the light of recent research into protein superfamilies from tick saliva. Our conclusions are that the main tick families adapted independently to a blood-feeding environment. This is supported by major differences observed in all processes involved with blood-feeding for hard and soft ticks. Gene duplication events played a major role in the evolution of novel protein functions involved in tick-host interactions. This occurred during the late Cretaceous and was stimulated by the radiation of birds and placental mammals, which provided numerous new niches for ticks to adapt to a new lifestyle. Independent adaptation of the main tick families to a blood-feeding environment has several implications for future tick research in terms of tick genome projects and vaccine development.     

Trends and rates of microevolution in plants

Evidence for rapid evolutionary change in plants in response to changing environmental conditions is widespread in the literature. However, evolutionary change in plant populations has not been quantified using a rate metric that allows for comparisons between and within studies. One objective of this paper is to estimate rates of evolution using data from previously published studies to begin a foundation for comparison and to examine trends and rates of microevolution in plants. We use data gathered from studies of plant adaptations in response to heavy metals, herbicide, pathogens, changes in pH, global change, and novel environments. Rates of evolution are estimated in the form of two metrics, darwins and haldanes. A second objective is to demonstrate how estimated rates could be used to address specific microevolutionary questions. For example, we examine how evolutionary rate changes with time, life history correlates of evolutionary rates, and whether some types of traits evolve faster than others. We also approach the question of how rates can be used to predict patterns of evolution under novel selection pressures using two contemporary examples: introductions of non-native species to alien environments and global change.     

Progress in risk assessment for classical biological control

There has been considerable debate on risks associated with biological control, and partly resulting from this, research has addressed a number of questions which have subsequently led to a greater understanding of risk assessment and biosafety. Controversy which arose in the 1980s about the environmental safety of biological control initially created considerable tension between biological control practitioners and those concerned about non-target impacts. Several factors have helped to ease this pressure, and a substantial body of research has addressed many of the questions raised. This has led to advances in quarantine laboratory host range testing to improve our ability to predict post-release impacts. Furthermore, pre- and post-release studies are increasingly involving population models to estimate the population impact of introduced biological control agents rather than simply measuring attack rates. Regulators making decisions about biological control agent introductions work under conditions of considerable uncertainty, but with accumulating data from past introductions to validate earlier decisions, and a robust peer review system for assessing new proposals, there is cause for some optimism that the risks associated with biological control can be better identified and managed in the future. Progress in research and regulation of biological control are discussed with particular reference to Australasia.     

What is macroevolution?

Definitions of macroevolution fall into three categories: (1) evolution of taxa of supraspecific rank; (2) evolution on the grand time-scale; and (3) evolution that is guided by sorting of interspecific variation (as opposed to sorting of intraspecific variation in microevolution). Here, it is argued that only definition 3 allows for a consistent separation of macroevolution and microevolution. Using this definition, speciation has both microevolutionary and macroevolutionary aspects: the process of morphological transformation is microevolutionary, but the variation among species that it produces is macroevolutionary, as is the rate at which speciation occurs. Selective agents may have differential effects on intraspecific and interspecific variation, with three possible situations: effect at one level only, effect at both levels with the same polarity but potentially different intensity, and effects that oppose between levels. Whereas the impact of all selective agents is direct in macroevolution, microevolution requires intraspecific competition as a mediator between selective agents and evolutionary responses. This mediating role of intraspecific competition occurs in the presence of sexual reproduction and has therefore no analogue at the macroevolutionary level where species are the evolutionary units. Competition between species manifests both on the microevolutionary and macroevolutionary level, but with different effects. In microevolution, interspecific competition spurs evolutionary divergence, whereas it is a potential driver of extinction at the macroevolutionary level. Recasting the Red Queen hypothesis in a macroevolutionary framework suggests that the effects of interspecific competition result in a positive correlation between origination and extinction rates, confirming empirical observations herein referred to as Stanley's rule.     

Biological control and sustainable food production

The use of biological control for the management of pest insects pre-dates the modern pesticide era. The first major successes in biological control occurred with exotic pests controlled by natural enemy species collected from the country or area of origin of the pest (classical control). Augmentative control has been successfully applied against a range of open-field and greenhouse pests, and conservation biological control schemes have been developed with indigenous predators and parasitoids. The cost-benefit ratio for classical biological control is highly favourable (1:250) and for augmentative control is similar to that of insecticides (1:2-1:5), with much lower development costs. Over the past 120 years, more than 5000 introductions of approximately 2000 non-native control agents have been made against arthropod pests in 196 countries or islands with remarkably few environmental problems. Biological control is a key component of a 'systems approach' to integrated pest management, to counteract insecticide-resistant pests, withdrawal of chemicals and minimize the usage of pesticides. Current studies indicate that genetically modified insect-resistant Bt crops may have no adverse effects on the activity or function of predators or parasitoids used in biological control. The introduction of rational approaches for the environmental risk assessment of non-native control agents is an essential step in the wider application of biological control, but future success is strongly dependent on a greater level of investment in research and development by governments and related organizations that are committed to a reduced reliance on chemical control.     

Exotic Lepidopteran Leafminers in North American Apple Orchards: Rise to Prominence, Management, and Future Threats

The European tentiform leafminers, Phyllonorycter blancardella (Fabricius) and P. mespilella (Hübner) (Lepidoptera: Gracillariidae), have infested apple, Malus domestica Borkhausen, in North America for at least 60–70 years. Unreliable taxonomic methods and lack of voucher specimens, however, have contributed to poor understanding of precisely when, where, and how these leafminers were introduced. Tentiform leafminers developed into significant foliar pests at about the time when adult resistance to broad-spectrum insecticides was detected in the 1970s and 1980s. At present, growers manage leafminers with insecticides and, to a lesser extent, with biological control. Most management programs for orchard pests rely on insecticides that are highly toxic to parasitic wasps, which hampers biological control. New techniques promoted in the context of integrated pest management (IPM) may improve biological control by reducing insecticidal use, but their adoption will depend on cost, labor, need to control other pests, and demands of the marketplace. Management programs must be flexible enough to accommodate changes in the species composition of leafminers and their parasitoids. Procedures to exclude pests may slow the rate of new introductions of leafminers and other pests, but they will not entirely protect the North American apple industry. Once new apple pests reach North America, they face few obstacles to further dispersal. The abundance of potential host plants, the lack of rigorous inspections, and new retail practices may facilitate the dispersal of exotic pests.