The evolutionary ecology of resistance to parasitoids by Drosophila

Parasitoids are the most important natural enemies of many insect species. Larvae of many Drosophila species can defend themselves against attack by parasitoids through a cellular immune response called encapsulation. The paper reviews recent studies of the evolutionary biology and ecological genetics of resistance in Drosophila, concentrating on D. melanogaster. The physiological basis of encapsulation, and the genes known to interfere with resistance are briefly summarized. Evidence for within- and between-population genetic variation in resistance from isofemale line, artificial selection and classical genetic studies are reviewed. There is now firm evidence that resistance is costly to Drosophila, and the nature of this cost is discussed, and the possibility that it may involve a reduction in metabolic rate considered. Comparative data on encapsulation and metabolic rates across seven Drosophila species provides support for this hypothesis. Finally, the possible population and community ecological consequences of evolution in the levels of host resistance are examined.

Tolerance traits and the stability of mutualism

Identifying factors which allow the evolution and persistence of cooperative interactions between species is a fundamental issue in evolutionary ecology. Various hypotheses have been suggested which generally focus on mechanisms that allow cooperative genotypes in different species to maintain interactions over space and time. Here, we emphasise the fact that even within mutualisms (interactions with net positive fitness effects for both partners), there may still be inherent costs, such as the occasional predation by ants upon aphids. Individuals engaged in mutualisms benefit from minimising these costs as long as it is not at the expense of breaking the interspecific interaction, which offers a net positive benefit. The most common and obvious defence traits to minimise interspecific interaction costs are resistance traits, which act to reduce encounter rate between two organisms. Tolerance traits, in contrast, minimise fitness costs to the actor, but without reducing encounter rate. Given that, by definition, it is beneficial to remain in mutualistic interactions, the only viable traits to minimise costs are tolerance-based 'defence' strategies. Thus, we propose that tolerance traits are an important factor promoting stability in mutualisms. Furthermore, because resistance traits tend to propagate coevolutionary arms races between antagonists, whilst tolerance traits do not, we also suggest that tolerance-based defence strategies may be important in facilitating the transition from antagonistic interactions into mutualisms. For example, the mutualism between ants and aphids has been suggested to have evolved from parasitism. We describe how phenotypic plasticity in honeydew production may be a tolerance trait that has prevented escalation into an antagonistic arms race and instead led to mutualistic coevolution.

Identification of trade-offs underlying the primary strategies of plants

Question: What are the key physiological and life-history trade-offs responsible for the evolution of different suites of plant traits (strategies) in different environments? Experimental methods: Common-garden experiments were performed on physiologically realistic model plants, evolved in contrasting environments, in computer simulations. This allowed the identification of the trade-offs that resulted in different suites of traits (strategies). The environments considered were: resource rich, low disturbance (competitive); resource poor, low disturbance (stressed); resource rich, high disturbance (disturbed); and stressed environments containing herbivores (grazed). Results: In disturbed environments, plants increased reproduction at the expense of ability to compete for light and nitrogen. In competitive environments, plants traded off reproductive output and leaf production for vertical growth. In stressed environments, plants traded off vertical growth and reproductive output for nitrogen acquisition, contradicting Grime's (2001) theory that slow-growing, competitively inferior strategies are selected in stressed environments. The contradiction is partly resolved by incorporating herbivores into the stressed environment, which selects for increased investment in defence, at the expense of competitive ability and reproduction. Conclusion: Our explicit modelling of trade-offs produces rigorous testable explanations of observed associations between suites of traits and environments.

The costs and consequences of parasitoid attack for the predatory hoverfly, Episyrphus balteatus

Question: What are the life-history costs for a predatory insect of surviving parasitoid attack, and can parasitoid attack alter predator-prey interactions? Hypotheses: Survivorship is influenced by host age. Hosts that suffer parasitoid attack grow more slowly and consume fewer prey. Those that survive attack are smaller as adults and show reduced survivorship. Organisms: The aphidophagous hoverfly Episyrphus balteatus, its endoparasitoid wasp Diplazon laetatorius and its prey, the pea aphid, Acyrthosiphon pisum. Site of experiments: All experiments were conducted in controlled temperature rooms and chambers in the laboratory. Methods: Episyrphus balteatus larvae of each instar were exposed to attack by Diplazon laetatorius, then dissected to measure the encapsulation response (a measure of immunity). Second instar larvae were either attacked or not attacked by D. laetatorius. Their development rates and numbers of prey consumed were noted. The size and survivorship of surviving (immune) and control hoverflies were compared following eclosion. Conclusions: Successful immune response increased with larval age (first instar 0%, second instar 40%, third instar 100% survival). Second instar larvae that successfully resisted parasitoid attack were larger as pupae (but not as adults) and showed reduced adult survivorship. Female adult survivors were more likely than male survivors to have died within 16 days of eclosion, but there was no difference between unattacked male and female control hoverflies. Attacked larvae, irrespective of immune status, consumed fewer aphids than unattacked individuals. Episyrphus balteatus suffers significant costs of resisting parasitoid attack, and parasitoid attack can reduce the top-down effects of an insect predator, irrespective of whether the host mounts an immune response or not.

Optimal growth strategies when mortality and production rates are size-dependent

Pontryagin's maximum principle from optimal control theory is used to find the optimal allocation of energy between growth and reproduction when lifespan may be finite and the trade-off between growth and reproduction is linear. Analyses of the optimal allocation problem to date have generally yielded bang-bang solutions, i.e. determinate growth: life-histories in which growth is followed by reproduction, with no intermediate phase of simultaneous reproduction and growth. Here we show that an intermediate strategy (indeterminate growth) can be selected for if the rates of production and mortality either both increase or both decrease with increasing body size, this arises as a singular solution to the problem. Our conclusion is that indeterminate growth is optimal in more cases than was previously realized. The relevance of our results to natural situations is discussed.

The short- and long-term fitness consequences of natal dispersal in a wild bird population

Dispersal is a key process in population and evolutionary ecology. Individual decisions are affected by fitness consequences of dispersal, but these are difficult to measure in wild populations. A long-term dataset on a geographically closed bird population, the Mauritius kestrel, offers a rare opportunity to explore fitness consequences. Females dispersed further when the availability of local breeding sites was limited, whereas male dispersal correlated with phenotypic traits. Female but not male fitness was lower when they dispersed longer distances compared to settling close to home. These results suggest a cost of dispersal in females. We found evidence of both short- and long-term fitness consequences of natal dispersal in females, including reduced fecundity in early life and more rapid aging in later life. Taken together, our results indicate that dispersal in early life might shape life history strategies in wild populations.

Managing threatened species – the ecological toolbox, evolutionary theory and the declining-population paradigm

1. The management of threatened species is an important practical way in which conservationists can intervene in the extinction process and reduce the loss of biodiversity. Understanding the causes of population declines (past, present and future) is pivotal to designing effective practical management. This is the declining-population paradigm identified by Caughley. 2. There are three broad classes of ecological tool used by conservationists to guide management decisions for threatened species: statistical models of habitat use, demographic models and behaviour-based models. Each of these is described here, illustrated with a case study and evaluated critically in terms of its practical application. 3. These tools are fundamentally different. Statistical models of habitat use and demographic models both use descriptions of patterns in abundance and demography, in relation to a range of factors, to inform management decisions. In contrast, behaviourbased models describe the evolutionary processes underlying these patterns, and derive such patterns from the strategies employed by individuals when competing for resources under a specific set of environmental conditions. 4. Statistical models of habitat use and demographic models have been used successfully to make management recommendations for declining populations. To do this, assumptions are made about population growth or vital rates that will apply when environmental conditions are restored, based on either past data collected under favourable environmental conditions or estimates of these parameters when the agent of decline is removed. As a result, they can only be used to make reliable quantitative predictions about future environments when a comparable environment has been experienced by the population of interest in the past. 5. Many future changes in the environment driven by management will not have been experienced by a population in the past. Under these circumstances, vital rates and their relationship with population density will change in the future in a way that is not predictable from past patterns. Reliable quantitative predictions about population-level responses then need to be based on an explicit consideration of the evolutionary processes operating at the individual level. 6. Synthesis and applications. It is argued that evolutionary theory underpins Caughley’s declining-population paradigm, and that it needs to become much more widely used within mainstream conservation biology. This will help conservationists examine critically the reliability of the tools they have traditionally used to aid management decision-making. It will also give them access to alternative tools, particularly when predictions are required for changes in the environment that have not been experienced by a population in the past.

The genome strikes back: The evolutionary importance of defence against mobile elements

Increasingly, we regard the genome as a site and source of genetic conflict. This fascinating 'bottom-up' view brings up appealing connections between genome biology and whole-organism ecology, in which populations of elements compete with one another in their genomic habitat. Unlike other habitats, though, a host genome has its own evolutionary interests and is often able to defend itself against molecular parasites. Most well-studied organisms employ strategies to protect their genomes against the harmful effects of genomic parasites, including methylation, various pathways of RNA interference, and more unusual tricks such as repeat induced point-mutation (RIP). These genome defence systems are not obscure biological curiosities, but fundamentally important to the integrity and cohesion of the genome, and exert a powerful influence on genome evolution.

Managing threatened species: the ecological toolbox, evolutionary theory and declining-population paradigm

1. The management of threatened species is an important practical way in which conservationists can intervene in the extinction process and reduce the loss of biodiversity. Understanding the causes of population declines (past, present and future) is pivotal to designing effective practical management. This is the declining-population paradigm identified by Caughley. 2. There are three broad classes of ecological tool used by conservationists to guide management decisions for threatened species: statistical models of habitat use, demographic models and behaviour-based models. Each of these is described here, illustrated with a case study and evaluated critically in terms of its practical application. 3. These tools are fundamentally different. Statistical models of habitat use and demographic models both use descriptions of patterns in abundance and demography, in relation to a range of factors, to inform management decisions. In contrast, behaviour-based models describe the evolutionary processes underlying these patterns, and derive such patterns from the strategies employed by individuals when competing for resources under a specific set of environmental conditions. 4. Statistical models of habitat use and demographic models have been used successfully to make management recommendations for declining populations. To do this, assumptions are made about population growth or vital rates that will apply when environmental conditions are restored, based on either past data collected under favourable environmental conditions or estimates of these parameters when the agent of decline is removed. As a result, they can only be used to make reliable quantitative predictions about future environments when a comparable environment has been experienced by the population of interest in the past. 5. Many future changes in the environment driven by management will not have been experienced by a population in the past. Under these circumstances, vital rates and their relationship with population density will change in the future in a way that is not predictable from past patterns. Reliable quantitative predictions about population-level responses then need to be based on an explicit consideration of the evolutionary processes operating at the individual level. 6. Synthesis and applications. It is argued that evolutionary theory underpins Caughley's declining-population paradigm, and that it needs to become much more widely used within mainstream conservation biology. This will help conservationists examine critically the reliability of the tools they have traditionally used to aid management decision-making. It will also give them access to alternative tools, particularly when predictions are required for changes in the environment that have not been experienced by a population in the past.

Post-genomics approaches towards monitoring changes within the microbial ecology of the gut

The human gut microbiota, comprising many hundreds of different microbial species, has closely co-evolved with its human host over the millennia. Diet has been a major driver of this co-evolution, in particular dietary non-digestible carbohydrates. This dietary fraction reaches the colon and becomes available for microbial fermentation, and it is in the colon that the great diversity of gut microorganisms resides. For the vast majority of our evolutionary history humans followed hunter-gatherer life-styles and consumed diets with many times more non-digestible carbohydrates, fiber and whole plant polyphenol rich foods than typical Western style diets today.

Forecasting extinction risk of ectotherms under climate warming: an evolutionary perspective

1. It has been postulated that climate warming may pose the greatest threat species in the tropics, where ectotherms have evolved more thermal specialist physiologies. Although species could rapidly respond to environmental change through adaptation, little is known about the potential for thermal adaptation, especially in tropical species. 2. In the light of the limited empirical evidence available and predictions from mutation-selection theory, we might expect tropical ectotherms to have limited genetic variance to enable adaptation. However, as a consequence of thermodynamic constraints, we might expect this disadvantage to be at least partially offset by a fitness advantage, that is, the ‘hotter-is-better’ hypothesis. 3. Using an established quantitative genetics model and metabolic scaling relationships, we integrate the consequences of the opposing forces of thermal specialization and thermodynamic constraints on adaptive potential by evaluating extinction risk under climate warming. We conclude that the potential advantage of a higher maximal development rate can in theory more than offset the potential disadvantage of lower genetic variance associated with a thermal specialist strategy. 4. Quantitative estimates of extinction risk are fundamentally very sensitive to estimates of generation time and genetic variance. However, our qualitative conclusion that the relative risk of extinction is likely to be lower for tropical species than for temperate species is robust to assumptions regarding the effects of effective population size, mutation rate and birth rate per capita. 5. With a view to improving ecological forecasts, we use this modelling framework to review the sensitivity of our predictions to the model’s underpinning theoretical assumptions and the empirical basis of macroecological patterns that suggest thermal specialization and fitness increase towards the tropics. We conclude by suggesting priority areas for further empirical research.