Jessica Cockburn, Guy Williams, Doug Downie, Terrence Bellingan, Kendall Crous, Taryn Goble and Nkosinathi Mazungula
When a plant or animal is introduced into a new habitat where previously it was not know to occur, it is known as an alien species, or non-indigenous. This simple act can have some devastating consequences. Here scientists put an evolutionary spin on these invasions.
Argentine ant attacking native harvester ant. Photo by Alex Wild
Although many introductions of non-indigenous species occur globally, it is estimated that only about one in a thousand will become invasive (not just establish but adversely impact native species and ecosystem function). But these few can have major impacts. Invasion of an ecosystem by non-indigenous species is thought to be the biggest threat to global biodiversity, second only to the far more devastating destruction of habitats and fragmentation of landscapes. The economic impact of invasive species of weeds, agricultural pests and plant pathogens has been estimated at U.S $125 billion per year in the United States alone. Most research involving invasive species focuses on ecological aspects of invasion and management, including biological control (a phenomenon explicitly involving introducing alien species). The evolutionary repercussions of introducing organisms into novel environments, and evolutionary processes at work during invasions have generally been overlooked.
Evolution is the change in the genetic composition of a population over time. In order to proceed, evolution requires variation in that genetic composition that affects the survival and reproductive capacity of an organism. Individuals with greater survival and more progeny, or offspring have more copies of their genes in the next generation and are said to be naturally selected.
Rapid evolution is the same process observed over a short period of time, within a human lifetime for example. Such rapid change usually occurs as a result of extreme selection pressure, as in the case of resistance of insects to insecticides, or great reductions in population size. Studies on alien perennial weeds and many insect invaders indicate that these processes occur often during introductions into new environments. One of the fundamental aspects of invasion is the "lag phase" undergone by a foreign species once it reaches the new habitat; the period of time after introduction while the population is small and undetected prior to growing large in numbers and becoming invasive. This lag period may be both a demographic and evolutionary event where the most competitive individuals reproduce rapidly and the genetic composition of the introduced population changes as it establishes and spreads.
Flexibility of a species to change morphology or behaviour without undergoing genetic change (phenotypic plasticity), specialized morphology or life-history traits, and release from natural enemies have long been postulated as reasons for the success of invasive species. Related to the enemy release hypothesis is a hypothesis that argues that under conditions of few or no natural enemies, plants rapidly evolve to become less defended but more competitive (evolution of increased competitive ability hypothesis). The genetic foundations for such characteristics and their responses to changing selection pressures are beginning to be uncovered to interesting effect. Increasing evidence from common garden experiments suggests that many invasive species undergo rapid evolution during the establishment and spread stages of invasion. As landscapes become more homogenized by human activities and climates change, the composition and distribution of genetic diversity will be changed by novel selection pressures. These will act on both invaders and natives alike.
A Case study: Evolution in the Argentine Ant
An example of this type of rapid evolution was demonstrated by Neil Tsutsui of the University of California Davis and Andrew Suarez in a paper in the journal Conservation Biology. These workers have attempted to decipher how the Argentine ant (Linepithema humile) has become such a successful invader in the USA. Instead of displaying the same territorial and aggressive behaviour towards ants from other nests and forming small colonies as they did in Argentina, in the USA these scientists observed "the formation of widespread colonies with numerous separate but interconnected nests, each containing many queens". By reducing intraspecific competition, there was a greater biomass and greater competitive ability in comparison to the local ant species.
From a combination of behavioural and molecular genetic studies they concluded that the lack of inter-nest aggression was due to a reduction in the genetic diversity of the ants (they don't recognise non-nestmates as such). The genetic similarity to one another makes them less likely to show aggression and territoriality, and so 'supercolonies' are formed. A similar pattern has been described in this species in Europe and may also be occurring in South Africa. According to the Global Invasive Species Database, the Argentine ant is an alien invasive species in South Africa, and poses a severe threat to the integrity of parts of the fynbos biome. Caroline Christian, then at the University of California, has shown how the Argentine ant is displacing native ants as dispersers of seeds of certain species of Proteacea. However they are inferior dispersers, and this has negative effects on the reproduction of the plants.
While low genetic diversity is implicated in the success of the Argentine ant, increased genetic variation is often the catalyst for rapid evolution and invasion. The introduction of the Cuban lizard (Anolis sagrei) to Florida is an example of how an introduced population can have increased rather than reduced genetic diversity. In this case, re-introductions of the species from multiple sources increased the genetic diversity and may have played a role in the species becoming more invasive. Previously unknown, highly invasive forms of reed canarygrass (Phalaris arundinacea) have emerged in the USA as a result of multiple introductions from genetically differentiated native populations from across Europe. Such multiple introductions may produce novel gene combinations with the potential to invade novel habitats. These examples illustrate how taking an evolutionary viewpoint of invasions can shed new light on old problems.
Invasions are not simply about invaders however, as shown in the fynbos example above. Native species interact with invaders and evolutionary responses are to be expected. Invasions can undoubtedly result in altered selection pressures on indigenous species. The potential for rapid evolution is therefore as applicable to native as invasive species. Many instances of genetically based adaptations of morphology and behavior in natives in response to invasive predators have been recorded. One of these is the soapberry bug (Jadera haematoloma) studied by Scott Carroll and colleagues which in 50 years has evolved significantly shorter beaks (mouthparts), as well as diverged in life history and physiological traits, in populations on an introduced host in Florida.
Evolution in Biological Control of Invasive Species
Biological control is touted as an ideal control measure for invasive species due to its apparent sustainability and benign environmental effects.
Biological control practitioners are understandably looking for a solution at fairly short time scales, to try and solve problems of invasions within human lifetimes. This does not take into account the effects of evolution, thought to be quite long-term and slow-moving in nature. Heinz Müller-Schärer and colleagues from the University of Fribourg in Switzerland point out that "evidence is increasing that invasive plants can undergo rapid evolution during the process of range expansion". They argue that evolutionary change which occurs during an invasion, or the expansion of a species' range, will affect the relationship between plants and their natural enemies. Because the plant will be exposed to more generalist and fewer specialist herbivores in the introduced range, selection could alter patterns of resource allocation, with more resources diverted to growth than defence, or plants flowering on multiple occasions throughout the year rather than one flowering event.
Houndstounge. Photo by Mary Ellen Harte
This increase in competitive ability has been observed in a number of species, for example in Cynoglossum officinale (Houndstounge), Senecio jacobea (Ragwort) and Digitalis purpurea (Common foxglove). This phenomenon has important implications for the effectiveness of biological control agents: if an invasive plant has newly evolved in the presence of generalists, then it may be vulnerable to specialist biocontrol agents. The role of evolution in biological control systems is also highlighted in a publication by Ruth Hufbauer and George Roderick, who take a theoretical approach to the question of biocontrol evolution, discussing it in relation to the four fundamental processes in evolution; mutation, genetic drift, selection and gene flow. The role of local adaptation is also discussed, a process which is fairly common in interactions between parasites/predators and hosts, which can influence the interaction between a biocontrol agent and its host. An important conclusion is reached by these authors: "for biological control to be an evolutionary stable means of managing pests there needs to be a balance between the evolution of resistance of target pests to their biological control agents, and evolution in biological control agents to overcome resistance". They state there is great potential for better understanding of biological control interactions from a microevolutionary perspective, but that data and experimental manipulations are needed for this.
The advantages of studying invasions through an evolutionary lens are compound. Firstly, investigations into the evolutionary impacts of human activities may provide information on the consequences of our actions in terms of speciation, aggravation of pest problems, erosion of genetic diversity and possibly changes to the evolutionary potential of various organisms. Secondly, although it seems unlikely at present, many researchers stress the potential predictive power stemming from an understanding of the evolutionary processes that underlie invasions.
It would be useful to infer the pace and direction of rapid evolution in the future. Biological control agents could be chosen with specific reference to their historical evolutionary relationship with a pest, predicted impact upon the evolution of the pest, and potential for subsequent evolution onto non-target hosts. We may in some ways be able to manipulate certain aspects of selection or genetic variation in order to manage pests and beneficial organisms, provided we understand the implications of doing so.
A literature search on the role of evolution in invasion of alien species in the South African context reveals that work in this field in South Africa is scant, and invasion biology is still highly focused on ecological processes. The opportunity to incorporate molecular genetic methods and take a more evolutionary approach to predicting and dealing with problems of invasive species remains to be explored, and has the potential to answer many questions on invasion biology in South Africa.