Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory

Useful ways of being wrong

Ecologists and evolutionary biologists have revealed that adaptive microevolution (i.e., allele frequency changes through time) and behavioral changes occur rapidly enough to affect contemporary ecological dynamics, and we can consider rapid adaptation for better conservation and management of wild populations. However, previous studies tended to focus on adaptation that increases population densities (e.g., evolutionary rescue), and did not pay attention to adaptation that decreases population densities (e.g., evolutionary suicide). Here, we demonstrate that controlling trait adaptation may be potentially important for decreasing population densities. One possibility is introducing “selfish” genotypes to populations. If the genotypes increase their reproductive success at the expense of population growth (e.g., cheaters in subsocial ants or coercive males in damselflies), we can decrease population densities (intraspecific adaptation load). The other possible option is diverting trait values of animals from the value that maximizes population growth (ecological trap). For example, we may be able to change behavior of a deer population by hunting so that they will not approach the best habitat with ample resources (landscape of fear). Then, we can consider the optimal allocation of our effort to directly decrease their population densities and control their trait values. However, we should carefully conduct controlling trait adaptation because it may result in unintended outcomes through modified genetic compositions and behaviors, such as increasing genetic variation of the focal population that enhances adaptation to changing environments by introducing selfish genotypes or a transient increase of population densities by modified behaviors.

Evolutionary suicide is a riveting phenomenon in which adaptive evolution drives a viable population to extinction. Gyllenberg and Parvinen (Bull Math Biol 63(5):981-993, 2001) showed that, in a wide class of deterministic population models, a discontinuous transition to extinction is a necessary condition for evolutionary suicide. An implicit assumption of their proof is that the invasion fitness of a rare strategy is well-defined also in the extinction state of the population. Epidemic models with frequency-dependent incidence, which are often used to model the spread of sexually transmitted infections or the dynamics of infectious diseases within herds, violate this assumption. In these models, evolutionary suicide can occur through a non-catastrophic bifurcation whereby pathogen adaptation leads to a continuous decline of host (and consequently pathogen) population size to zero. Evolutionary suicide of pathogens with frequency-dependent transmission can occur in two ways, with pathogen strains evolving either higher or lower virulence.

One of the most pressing questions we face as biologists is to understand how climate change will affect the evolutionary dynamics of natural populations and how these dynamics will in turn affect population recovery. Increasing evidence shows that sexual selection favors population viability and local adaptation. However, sexual selection can also foster sexual conflict and drive the evolution of male harm to females. Male harm is extraordinarily widespread and has the potential to suppress female fitness and compromise population growth, yet we currently ignore its net effects across taxa or its influence on local adaptation and evolutionary rescue. We conducted a comparative meta-analysis to quantify the impact of male harm on female fitness and found an overall negative effect of male harm on female fitness. Negative effects seem to depend on proxies of sexual selection, increasing inversely to the female relative size and in species with strong sperm competition. We then developed theoretical models to explore how male harm affects adaptation and evolutionary rescue. We show that, when sexual conflict depends on local adaptation, population decline is reduced, but at the cost of slowing down genetic adaptation. This trade-off suggests that eco-evolutionary feedback on sexual conflict can act like a double-edged sword, reducing extinction risk by buffering the demographic costs of climate change, but delaying genetic adaptation. However, variation in the mating system and male harm type can mitigate this trade-off. Our work shows that male harm has widespread negative effects on female fitness and productivity, identifies potential mechanistic factors underlying variability in such costs across taxa, and underscores how acknowledging the condition-dependence of male harm may be important to understand the demographic and evolutionary processes that impact how species adapt to environmental change.

Adaptive evolution of body size subject to indirect effect in trophic cascade system

Evolution between two competing macrophyte populations along a resource gradient leads to collapse in a bistable lake ecosystem.

Speciation occurs when a population splits into ecologically differentiated and reproductively isolated lineages. In this chapter, we focus on the ecological side of nonallopatric speciation: Under what ecological conditions is speciation promoted by natural selection? What are the appropriate tools to identify speciation-prone ecological systems? For speciation to occur, a population must have the potential to become polymorphic (i.e., it must harbor heritable variation). Moreover, this variation must be under disruptive selection that favors extreme phenotypes at the cost of intermediate ones. With disruptive selection, a genetic polymorphism can be stable only if selection is frequency dependent (Pimm 1979; see Chapter 3). Some appropriate form of frequency dependence is thus an ecological prerequisite for nonallopatric speciation. Frequency-dependent selection is ubiquitous in nature. It occurs, among many other examples, in the context of resource competition (Christiansen and Loeschcke 1980; see Box 4.1), predator–prey systems (Marrow et al. 1992), multiple habitats (Levene 1953), stochastic environments (Kisdi and Meszena 1993; Chesson 1994), asymmetric competition (Maynard Smith and Brown 1986), mutualistic interactions (Law and Dieckmann 1998), and behavioral conflicts (Maynard Smith and Price 1973; Hofbauer and Sigmund 1990). The theory of adaptive dynamics is a framework devised to model the evolution of continuous traits driven by frequency-dependent selection. It can be applied to various ecological settings and is particularly suitable for incorporating ecological complexity. The adaptive dynamic analysis reveals the course of long-term evolution expected in a given ecological scenario and, in particular, shows whether, and under which conditions, a population is expected to evolve toward a state in which disruptive selection arises and promotes speciation. To achieve analytical tractability in ecologically complex models, many adaptive dynamic models (and much of this chapter) suppress genetic complexity with the assumption of clonally reproducing phenotypes (also referred to as strategies or traits). This enables the efficient identification of interesting features of the engendered selective pressures that deserve further analysis from a genetic perspective.

Does the evolution of self-fertilization rescue populations or increase the risk of extinction?

Populations facing novel environments can persist by adapting. In nature, the ability to adapt and persist will depend on interactions between coexisting individuals. Here we use an adaptive dynamic model to assess how the potential for evolutionary rescue is affected by intra- and interspecific competition. Intraspecific competition (negative density-dependence) lowers abundance, which decreases the supply rate of beneficial mutations, hindering evolutionary rescue. On the other hand, interspecific competition can aid evolutionary rescue when it speeds adaptation by increasing the strength of selection. Our results clarify this point and give an additional requirement: competition must increase selection pressure enough to overcome the negative effect of reduced abundance. We therefore expect evolutionary rescue to be most likely in communities which facilitate rapid niche displacement. Our model, which aligns to previous quantitative and population genetic models in the absence of competition, provides a first analysis of when competitors should help or hinder evolutionary rescue.

Hyperparasitism denotes the natural phenomenon where a parasite infecting a host is in turn infected by its own parasite. Hyperparasites can shape the dynamics of host-parasite interactions and often have a deleterious impact on pathogens, an important class of parasites, causing a reduction in their virulence and transmission rate. Hyperparasitism thus could be an important tool of biological control. However, host-parasite-hyperparasite systems have so far been outside the mainstream of modeling studies, especially those dealing with eco-evolutionary aspects of species interactions. Here, we theoretically explore the evolution of life-history traits in a generic host-parasite-hyperparasite system, focusing on parasite virulence and the positive impact that hyperparasitism has on the host population. We also explore the coevolution of life-history traits of the parasite and hyperparasite, using adaptive dynamics and quantitative genetics frameworks to identify evolutionarily singular strategies. We find that in the presence of hyperparasites, the evolutionarily optimal pathogen virulence generally shifts toward more virulent strains. However, even in this case the use of hyperparasites in biocontrol could be justified, since overall host mortality decreases. An intriguing possible outcome of the evolution of the hyperparasite can be its evolutionary suicide.

Theory suggests that a population with a narrower niche can adapt more rapidly to environmental change, all else being equal. However, a narrow niche may be correlated with other factors that compromise evolvability, such as a smaller population size, and it is unclear if specialist mutants can succeed by virtue of greater evolvability when impeded by the ecological costs of a narrower niche. Here, we use simulation models to show that specialist mutants can invade during periods of rapid environmental change, in some cases preventing extinction. Focusing on asexual populations, we show that successful specialist mutants typically enjoy 2 types of advantages over generalists: an immediate benefit of ignoring a habitat in which they are particularly unfit and a longer-term benefit of greater evolvability. By understanding the mechanisms that yield these benefits, we are also able to show that evolutionary rescue by specialization can be largely prevented by manipulating the schedule of environmental change. Our results demonstrate how a population may change fundamentally under strong pressure to adapt rapidly, with implications for both beneficial (e.g., conservation) and harmful (e.g., antibiotic resistance) examples of evolutionary rescue.

Global warming is severely impacting ecosystems and threatening ecosystem services as well as human well-being. While some species face extinction risk, several studies suggest the possibility that fast evolution may allow species to adapt and survive in spite of environmental changes. We assess how such evolutionary rescue extends to multitrophic communities and whether evolution systematically preserves biodiversity under global warming. More precisely, we expose simulated trophic networks of co-evolving consumers to warming under different evolutionary scenarios, which allows us to assess the effect of evolution on diversity maintenance. We also investigate how the evolution of body mass and feeding preference affects coexistence within a simplified consumer-resource module. Our simulations predict that the long-term diversity loss triggered by warming is considerably higher in scenarios where evolution is slowed down or switched off completely, indicating that eco-evolutionary feedback indeed helps to preserve biodiversity. However, even with fast evolution, food webs still experience vast disruptions in their structure and functioning. Reversing warming may thus not be sufficient to restore previous structures. Our findings highlight how the interaction between evolutionary rescue and changes in trophic structures constrains ecosystem responses to warming with important implications for conservation and management policies.

Recent studies have revealed the importance of feedbacks between contemporary rapid evolution (i.e. evolution that occurs through changes in allele frequencies) and ecological dynamics. Despite its inherent interdisciplinary nature, however, studies on eco-evolutionary feedbacks have been mostly ecological and tended to focus on adaptation at the phenotypic level without considering the genetic architecture of evolutionary processes. In empirical studies, researchers have often compared ecological dynamics when the focal species under selection has a single genotype with dynamics when it has multiple genotypes. In theoretical studies, common approaches are models of quantitative traits where mean trait values change adaptively along the fitness gradient and Mendelian traits with two alleles at a single locus. On the other hand, it is well known that genetic architecture can affect short-term evolutionary dynamics in population genetics. Indeed, recent theoretical studies have demonstrated that genetic architecture (e.g. the number of loci, linkage disequilibrium and ploidy) matters in eco-evolutionary dynamics (e.g. evolutionary rescue where rapid evolution prevents extinction and population cycles driven by (co)evolution). I propose that theoretical approaches will promote the synthesis of functional genomics and eco-evolutionary dynamics through models that combine population genetics and ecology as well as nonlinear time-series analyses using emerging big data.This article is part of the theme issue ‘Genetic basis of adaptation and speciation: from loci to causative mutations’.

Summary The European Water Framework Directive (WFD) requires that all natural European waterbodies should be assigned to one of five ecological categories defining the degree to which present‐day conditions deviate from those uninfluenced or only negligibly impacted by anthropogenic activities (the reference condition). By 2015, all relevant waterbodies must have obtained ‘good’ ecological quality. We describe the changes in ecological state in 21 Danish lakes using ad 1850 as a benchmark for reference conditions. Sediment samples representing 1850, 1900, 1950 and 2000 were analysed for diatom and cladoceran subfossils. Ecological status since 1850 was evaluated using correspondence analysis and dissimilarity measures to assess assemblage changes, and existing transfer functions were applied to infer changes in total phosphorous concentrations from diatoms (DI‐TP) and submerged macrophyte coverage (SUB‐COV) and benthi‐planktivorous fish catch per unit effort (BP‐CPUE) from cladoceran subfossils. Eighteen lakes underwent significant changes, most markedly during the past 50–100 years, in either or both diatom and cladoceran community structure. Low floristic and faunal alteration was found only in three lakes; these were, however, already nutrient‐rich in 1850. In 1850, most lakes were already characterized by high DI‐TP (median of 17 lakes = 86 µg TP L−1), high inferred BP‐CPUE and low inferred SUB‐COV, and these eutrophic conditions still prevail. In addition, the accumulation rate of sediment and cladoceran subfossils and the pelagic dominance of diatoms and cladocerans have increased. When applying the thresholds proposed by a recent WFD classification for Danish lakes to the DI‐TP values, only one lake could be described as having a ‘good’ ecological state with a concurrent low community change since 1850, limited to the cladoceran community, however. This suggests that this lake alone may serve as a potential reference site. Synthesis and applications. Our study, demonstrating the potential of a palaeolimnological approach to assess deviations from reference conditions, suggests that Danish reference lakes may be difficult to find, most probably due to the country's long history of cultural impact. Lake managers consequently face great challenges in their endeavour to ensure ‘good’ ecological state by 2015. Therefore, further restrictions on land‐use and nutrient loading in lake catchments are needed as is the initiation of restoration activities to improve the ecological state of the lakes.

Populations that experience severe stress may avoid extinction through adaptation by natural selection. This process is called evolutionary rescue and has been studied under different names in medicine, agriculture, and conservation biology. It is a component of the emerging field of eco-evolutionary dynamics, which investigates how the ecological attributes of species may evolve rapidly under strong selection. Its distinguishing feature is to combine the evolutionary concept of relative fitness with the ecological concept of absolute fitness in a synthetic theory of persistent adaptation. The likelihood of rescue will depend both on attributes of the population, particularly abundance and variation, and on properties of the environment, particularly the rate and severity of deterioration. Medical interventions (e.g., the administration of antibiotics), agricultural practices (e.g., the application of pesticides), and population ecology (e.g., the effects of species introductions) provide numerous examples of evolutionary rescue. The general theory of rescue has been tested in laboratory experiments with microbes, in which experimental evolution shows how different treatments affect the frequency of rescue. Overall, these experiments have supported the predictions of general theory: In particular, abundance, variation, and dispersal have pronounced and repeatable effects on the rescue of populations and communities. Extending these laboratory results to the field is a major task for future research.