Photo: Kochia in Southwestern Montana. © 2020 Delena Norris-Tull
Evolutionary Changes in the New Environment: Potential impacts on the effectiveness of biocontrol agents
Summaries of the research and commentary by Dr. Delena Norris-Tull, Professor Emerita of Science Education, University of Montana Western, September 2020.
Müller-Scharer, et al., 2004, conducted a review of the research on evolution that may occur in invasive plants within their new non-native range. They found that, “Two contrasting, but mutually non-exclusive hypotheses address the relationship between phenotype and invasion success; the first assumes that invaders are pre-adapted with traits that make them successful invaders, whereas the second postulates successful invasion as the outcome of rapid evolutionary change once the species has become established in the new habitat.”
They also found that, “Many of the best examples of rapid evolution involve invasive plants, possibly because of the genetic processes involved during invasion that enhance genetic variation (on which selection can act; including hybridization), or to strong directional selection exerted by abiotic and/or biotic factors. Interactions with competitors and natural enemies differs strongly between the native and introduced range. If evolutionary change does occur, knowledge of its pace and direction might help to improve our predictions of the impact of subsequent biological control attempts.”
[Within this website, refer to the section on Herbicide Resistance, for description of the rapid evolution of invasive plant species in response to the selective pressure resulting from the use of herbicides.]
Müller-Scharer, et al., 2004, also found that, “The enemy release hypothesis posits that introduced plants experience a decrease in regulation by herbivores and other natural enemies, and, therefore, can spread rapidly. It has been shown that invasive exotic plants do suffer a reduced overall amount of herbivore damage, or are attacked by fewer herbivorous invertebrates, fungal and viral pathogens compared with the same species in their native range.” This reduction of damage is primarily due to the fact that the plants no longer can be attacked by their specialist enemies from their home range. “However, the level of attack by local [native] generalists can vary considerably, and can even hinder the invasion of certain communities.” Müller-Scharer, et al., 2004, propose that “the most prominent change experienced by introduced plants in terms of natural enemies is a shift in the composition toward an assemblage that is dominated by generalists. Attack by specialists is restricted to those cases in which natural enemies feeding on closely related natives colonize the introduced plant, or where specialist herbivores have been co-introduced. The shift in the composition of the natural enemy complex in the exotic range, along with changes in the competitive environment and in resource availability, is expected to incur altered selection on traits in invasive plants.”
Müller-Scharer, et al., 2004, also noted that, “The EICA [evolution of increased competitive ability] hypothesis assumes that plant defence chemicals incur fitness costs. For qualitative defense (toxins such as alkaloids and glucosinolates), only a few of the many experimental studies on this topic found significant direct (allocation) costs. By contrast, quantitative defence compounds (e.g. lignins and tannins) appear to incur high costs because they constrain the inherit relative growth rate of plants… In the native range, different antagonists are expected, based on optimal defence theory, to impose differential selection on both the qualitative and quantitative defence traits of plants. First, high concentrations of plant toxins might deter generalists while attracting specialists that either use them as a cue to locate or to accept the host plant for oviposition and/or feeding or that sequester the toxins and use them for their own defence… As a result of opposite selection imposed by specialist and generalist herbivores, we expect plants to evolve intermediate levels of toxins….
“Second, plant species or genotypes that have lower quantitative defence are more susceptible to specialists and to those generalists that have adapted to the toxins of the plant, but… such defenses constrain the growth of the plant. Furthermore, interspecific studies revealed relative growth rate to be positively correlated with competitive ability and the risk of invasiveness. Thus, in the native range, selection exerted primarily by specialist natural enemies and plant competitors is expected to favour intermediate levels of quantitative defences.”
“In the introduced range, where specialist herbivores are largely absent, but plants might be attacked by native generalist herbivores, we expect that plant toxins will increase in concentration, rather than decrease as predicted by the EICA hypothesis. This is because high concentrations of toxins no longer have fitness costs associated with attracting or increasing the survival of specialist herbivores. Furthermore, there is increasing evidence that some plant toxins, including glucosinolates, also function to benefit plants in competitive interactions through allelopathic effects. Thus, an increase in their concentration might further enhance the potential of a population to become invasive. However, concentrations of lignins and/or tannins are expected to decrease, particularly when generalists in the introduced range are repelled by the plant toxins.
“Therefore, we propose that the evolved increased vigour documented in the introduced range for a few plant species is best explained by a reallocation of resources from costly quantitative defences to growth, whereas the toxin concentrations might well evolve in the opposite direction than that predicted by the EICA hypothesis. We suggest that such plants will be particularly amenable to biological control, because target weeds with increased digestibility are likely to support a faster population build-up of specialist biocontrol agents.”
Müller-Scharer, et al., 2004, found that little research had been conducted to study whether invasive plant populations are evolving tolerance as a response to attack. “What evolutionary trajectory do we expect in the introduced range where the intensity of competition and herbivory can be altered compared with the native range? Tolerance might be a defence mechanism that is particularly important for plant species that lack efficient chemical defence. Assuming that tolerance incurs fitness costs…, we might expect the evolution of decreased tolerance but increased competitive ability when plants are introduced into a new range… However, various factors might limit such an evolutionary response. First, selection imposed by generalist insect herbivores might be strong enough to maintain high tolerance in the introduced range. Second, it is likely that other stress and disturbance factors (e.g. fire, frost, or drought), which also operate in the introduced range, will lead to the maintenance of tolerance due to herbivory, because similar compensatory mechanisms might be activated after the destruction of apical meristems… by various abiotic stress and disturbance factors. Third, many introduced plants invade grassland habitats, where they are browsed by cattle. Thus, although in such habitats invasive plants might face lower levels of insect herbivory compared with their native range, browsing by cattle might nevertheless be common and impose strong selection on plant tolerance.”
Müller-Scharer, et al., 2004, stated that, “Therefore, effective tolerance mechanisms could be common in plant invaders. We propose that this can help explain why most introductions of insect biological control agents exhibit only weak negative effects on their hosts. It might further explain the resulting super-abundance of some of the biological control agents over extended time periods because tolerance, unlike resistance, is generally not expected to regulate the population dynamics of its consumers.” Müller-Scharer, et al., 2004, included, as one example, the two introduced gallfies that have failed to control Centaurea maculosa but now occur at a very high density compared to their native range.
Zenni, et al., 2017, conducted an extensive review of the research on the evolutionary processes that may impact the success of biological invasions by trees, to better understand the importance of the changes that invasive species undergo after being introduced to a new environment.
Ellstrand and Schierenbeck, 2000, point out that the fact that some species are readily controlled by biological agents brought over from their home environment is an indicator that evolution occurring after introduction is not a factor for those species. But the fact that various invasive species do not respond well to biocontrol presents the possibility that evolutionary changes occurring within the species within the new environment are an important factor, particularly among plant species.
[Within this website, refer to the section, Invasive Success Hypotheses, for details of the EICA, evolution of increased competitive ability hypothesis, and for more details of the research on hybridization.]
References:
Next Sections on Biocontrol Agents:
Evolutionary Changes in the New Environment: Potential impacts on the effectiveness of biocontrol agents
Summaries of the research and commentary by Dr. Delena Norris-Tull, Professor Emerita of Science Education, University of Montana Western, September 2020.
Müller-Scharer, et al., 2004, conducted a review of the research on evolution that may occur in invasive plants within their new non-native range. They found that, “Two contrasting, but mutually non-exclusive hypotheses address the relationship between phenotype and invasion success; the first assumes that invaders are pre-adapted with traits that make them successful invaders, whereas the second postulates successful invasion as the outcome of rapid evolutionary change once the species has become established in the new habitat.”
They also found that, “Many of the best examples of rapid evolution involve invasive plants, possibly because of the genetic processes involved during invasion that enhance genetic variation (on which selection can act; including hybridization), or to strong directional selection exerted by abiotic and/or biotic factors. Interactions with competitors and natural enemies differs strongly between the native and introduced range. If evolutionary change does occur, knowledge of its pace and direction might help to improve our predictions of the impact of subsequent biological control attempts.”
[Within this website, refer to the section on Herbicide Resistance, for description of the rapid evolution of invasive plant species in response to the selective pressure resulting from the use of herbicides.]
Müller-Scharer, et al., 2004, also found that, “The enemy release hypothesis posits that introduced plants experience a decrease in regulation by herbivores and other natural enemies, and, therefore, can spread rapidly. It has been shown that invasive exotic plants do suffer a reduced overall amount of herbivore damage, or are attacked by fewer herbivorous invertebrates, fungal and viral pathogens compared with the same species in their native range.” This reduction of damage is primarily due to the fact that the plants no longer can be attacked by their specialist enemies from their home range. “However, the level of attack by local [native] generalists can vary considerably, and can even hinder the invasion of certain communities.” Müller-Scharer, et al., 2004, propose that “the most prominent change experienced by introduced plants in terms of natural enemies is a shift in the composition toward an assemblage that is dominated by generalists. Attack by specialists is restricted to those cases in which natural enemies feeding on closely related natives colonize the introduced plant, or where specialist herbivores have been co-introduced. The shift in the composition of the natural enemy complex in the exotic range, along with changes in the competitive environment and in resource availability, is expected to incur altered selection on traits in invasive plants.”
Müller-Scharer, et al., 2004, also noted that, “The EICA [evolution of increased competitive ability] hypothesis assumes that plant defence chemicals incur fitness costs. For qualitative defense (toxins such as alkaloids and glucosinolates), only a few of the many experimental studies on this topic found significant direct (allocation) costs. By contrast, quantitative defence compounds (e.g. lignins and tannins) appear to incur high costs because they constrain the inherit relative growth rate of plants… In the native range, different antagonists are expected, based on optimal defence theory, to impose differential selection on both the qualitative and quantitative defence traits of plants. First, high concentrations of plant toxins might deter generalists while attracting specialists that either use them as a cue to locate or to accept the host plant for oviposition and/or feeding or that sequester the toxins and use them for their own defence… As a result of opposite selection imposed by specialist and generalist herbivores, we expect plants to evolve intermediate levels of toxins….
“Second, plant species or genotypes that have lower quantitative defence are more susceptible to specialists and to those generalists that have adapted to the toxins of the plant, but… such defenses constrain the growth of the plant. Furthermore, interspecific studies revealed relative growth rate to be positively correlated with competitive ability and the risk of invasiveness. Thus, in the native range, selection exerted primarily by specialist natural enemies and plant competitors is expected to favour intermediate levels of quantitative defences.”
“In the introduced range, where specialist herbivores are largely absent, but plants might be attacked by native generalist herbivores, we expect that plant toxins will increase in concentration, rather than decrease as predicted by the EICA hypothesis. This is because high concentrations of toxins no longer have fitness costs associated with attracting or increasing the survival of specialist herbivores. Furthermore, there is increasing evidence that some plant toxins, including glucosinolates, also function to benefit plants in competitive interactions through allelopathic effects. Thus, an increase in their concentration might further enhance the potential of a population to become invasive. However, concentrations of lignins and/or tannins are expected to decrease, particularly when generalists in the introduced range are repelled by the plant toxins.
“Therefore, we propose that the evolved increased vigour documented in the introduced range for a few plant species is best explained by a reallocation of resources from costly quantitative defences to growth, whereas the toxin concentrations might well evolve in the opposite direction than that predicted by the EICA hypothesis. We suggest that such plants will be particularly amenable to biological control, because target weeds with increased digestibility are likely to support a faster population build-up of specialist biocontrol agents.”
Müller-Scharer, et al., 2004, found that little research had been conducted to study whether invasive plant populations are evolving tolerance as a response to attack. “What evolutionary trajectory do we expect in the introduced range where the intensity of competition and herbivory can be altered compared with the native range? Tolerance might be a defence mechanism that is particularly important for plant species that lack efficient chemical defence. Assuming that tolerance incurs fitness costs…, we might expect the evolution of decreased tolerance but increased competitive ability when plants are introduced into a new range… However, various factors might limit such an evolutionary response. First, selection imposed by generalist insect herbivores might be strong enough to maintain high tolerance in the introduced range. Second, it is likely that other stress and disturbance factors (e.g. fire, frost, or drought), which also operate in the introduced range, will lead to the maintenance of tolerance due to herbivory, because similar compensatory mechanisms might be activated after the destruction of apical meristems… by various abiotic stress and disturbance factors. Third, many introduced plants invade grassland habitats, where they are browsed by cattle. Thus, although in such habitats invasive plants might face lower levels of insect herbivory compared with their native range, browsing by cattle might nevertheless be common and impose strong selection on plant tolerance.”
Müller-Scharer, et al., 2004, stated that, “Therefore, effective tolerance mechanisms could be common in plant invaders. We propose that this can help explain why most introductions of insect biological control agents exhibit only weak negative effects on their hosts. It might further explain the resulting super-abundance of some of the biological control agents over extended time periods because tolerance, unlike resistance, is generally not expected to regulate the population dynamics of its consumers.” Müller-Scharer, et al., 2004, included, as one example, the two introduced gallfies that have failed to control Centaurea maculosa but now occur at a very high density compared to their native range.
Zenni, et al., 2017, conducted an extensive review of the research on the evolutionary processes that may impact the success of biological invasions by trees, to better understand the importance of the changes that invasive species undergo after being introduced to a new environment.
Ellstrand and Schierenbeck, 2000, point out that the fact that some species are readily controlled by biological agents brought over from their home environment is an indicator that evolution occurring after introduction is not a factor for those species. But the fact that various invasive species do not respond well to biocontrol presents the possibility that evolutionary changes occurring within the species within the new environment are an important factor, particularly among plant species.
[Within this website, refer to the section, Invasive Success Hypotheses, for details of the EICA, evolution of increased competitive ability hypothesis, and for more details of the research on hybridization.]
References:
- Ellstrand, N.C., & Schierenbeck, K.A. (Jan. 27-29, 2000). Hybridization as a stimulus for the evolution of invasiveness in plants? Paper presented at the National Academy of Sciences, Irvine, CA. Reprinted in Euphytica (2006), 148, 35-46.
- Müller-Scharer, H., Schaffner, U., & Steinger, T. (August, 2004). Evolution in invasive plants: Implications for biological control. Trends in Ecology and Evolution, 19 (8), 417-422.
- Zenni, R.D., Dickie, I.A., Wingfield, M.J., Hirsch, H., Crous, C.J., Meyerson, L.A., Burgess, T.I., Zimmermann, T.G., Klock, M.M., Siemann, E., Erfmeier, A., Aragon, R., Montti, L, & LeRoux, J.J. (Jan., 2017). Evolutionary dynamics of tree invasions: Complementing the unified framework for biological invasions. AoB Plants, 9 (1), 1-14.
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