Hot spots become cold spots: coevolution in variable temperature environments.

Antagonistic coevolution between hosts and parasites is a key process in the genesis and maintenance of biological diversity. Whereas coevolutionary dynamics show distinct patterns under favourable environmental conditions, the effects of more realistic, variable conditions are largely unknown. We investigated the impact of a fluctuating environment on antagonistic coevolution in experimental microcosms of Pseudomonas fluorescens SBW25 and lytic phage SBWΦ2. High-frequency temperature fluctuations caused no deviations from typical coevolutionary arms race dynamics. However, coevolution was stalled during periods of high temperature under intermediate- and low-frequency fluctuations, generating temporary coevolutionary cold spots. Temperature variation affected population density, providing evidence that eco-evolutionary feedbacks act through variable bacteria-phage encounter rates. Our study shows that environmental fluctuations can drive antagonistic species interactions into and out of coevolutionary cold and hot spots. Whether coevolution persists or stalls depends on the frequency of change and the environmental optima of both interacting players.

What limits the evolutionary emergence of pathogens?

The ability of a pathogen to cause an epidemic when introduced in a new host population often relies on its ability to adapt to this new environment. Here, we give a brief overview of recent theoretical and empirical studies of such evolutionary emergence of pathogens. We discuss the effects of several ecological and genetic factors that may affect the likelihood of emergence: migration, life history of the infectious agent, host heterogeneity, and the rate and effects of mutations. We contrast different modelling approaches and indicate how details in the way we model each step of a life cycle can have important consequences on the predicted probability of evolutionary emergence. These different theoretical perspectives yield important insights into optimal surveillance and intervention strategies, which should aim for a reduction in the emergence (and re-emergence) of infectious diseases.

Persistence of costly novel genes in the absence of positive selection.

Many genetic changes that ultimately lead to adaptive evolution come with a short-term cost expressed in terms of reduced survival and reproduction. In the absence of genetic drift, it is unclear how such costly mutations may persist. Here we experimentally demonstrate that parasites can promote the persistence of costly genetic variants. We employed a genetically engineered strain (GMMO) of the bacterium Pseudomonas fluorescens as a model of the acquisition of a new gene either through a major mutation or through horizontal transfer, and examined its persistence in different evolving communities comprising an ancestral strain and a lytic bacteriophage. Whereas competition resulted in the elimination of the GMMO, inclusion of the phage promoted GMMO persistence. We provide evidence for why this effect is due to the differential susceptibility of GMMO and ancestral bacteria to phage.

Diversity and productivity peak at intermediate dispersal rate in evolving metacommunities.

Positive relationships between species diversity and productivity have been reported for a number of ecosystems. Theoretical and experimental studies have attempted to determine the mechanisms that generate this pattern over short timescales, but little attention has been given to the problem of understanding how diversity and productivity are linked over evolutionary timescales. Here, we investigate the role of dispersal in determining both diversity and productivity over evolutionary timescales, using experimental metacommunities of the bacterium Pseudomonas fluorescens assembled by divergent natural selection. We show that both regional diversity and productivity peak at an intermediate dispersal rate. Moreover, we demonstrate that these two patterns are linked: selection at intermediate rates of dispersal leads to high niche differentiation between genotypes, allowing greater coverage of the heterogeneous environment and a higher regional productivity. We argue that processes that operate over both ecological and evolutionary timescales should be jointly considered when attempting to understand the emergence of ecosystem-level properties such as diversity-function relationships.

Defence against multiple enemies.

Although very common under natural conditions, the consequences of multiple enemies (parasites, predators, herbivores, or even 'chemical' enemies like insecticides) on investment in defence has scarcely been investigated. In this paper, we present a simple model of the joint evolution of two defences targeted against two enemies. We illustrate how the respective level of each defence can be influenced by the presence of the two enemies. Furthermore, we investigate the influences of direct interference and synergy between defences. We show that, depending on certain conditions (costs, interference or synergy between defences), an increase in selection pressure by one enemy can have dramatic effects on defence against another enemy. It is generally admitted that increasing the encounter rate with a second natural enemy can decrease investment in defence against a first enemy, but our results indicate that it may sometimes favour resistance against the first enemy. Moreover, we illustrate that the global defence against one enemy can be lower when only this enemy is present: this has important implications for experimental measures of resistance, and for organisms that invade an area with less enemies or whose community of enemies is reduced. We discuss possible implications of the existence of multiple enemies for conservation biology, biological control and chemical control.

Modelling the spatial configuration of refuges for a sustainable control of pests: a case study of Bt cotton.

The 'high-dose-refuge' (HDR) strategy is widely recommended by the biotechnology industry and regulatory authorities to delay pest adaptation to transgenic crops that produce Bacillus thuringiensis (Bt) toxins. This involves cultivating nontoxic plants (refuges) in close proximity to crops producing a high dose of Bt toxin. The principal cost associated with this strategy is due to yield losses suffered by farmers growing unprotected, refuge plants. Using a population genetic model of selection in a spatially heterogeneous environment, we show the existence of an optimal spatial configuration of refuges that could prevent the evolution of resistance whilst reducing the use of costly refuges. In particular, the sustainable control of pests is achievable with the use of more aggregated distributions of nontransgenic plants and transgenic plants producing lower doses of toxin. The HDR strategy is thus suboptimal within the context of sustainable agricultural development.

Population genetics and dynamics of the black truffle in a man-made truffle field.

The colonization dynamics of the black truffle in an artificial field were assessed through analyses of microsatellite and RAPD markers. The truffle field was composed of three tree species and mycelial inoculum of three different origins, and was monitored for the first three years of truffle production. We found very low levels of genetic diversity. Isolation by distance was detected only at the between-tree level. This could be interpreted as local colonization around each tree facilitated by the presence of the tree root system. At the larger spatial scale of the European range, the absence of isolation by distance corroborates the hypothesis of an impact of glaciation on genetic variation, followed by rapid postglaciation demographic expansion. In addition, genetic variation of harvested truffles was explained by neither inoculation origin, nor tree species. Our study questions the real impact of man-made inoculation of tree root systems with fungal mycelia.

Disease diversity and human fertility.

The existence of parasitic constraints on the evolution of life-history traits in free-living organisms has been demonstrated in several plant and animal species. However, the association between different diseases and human traits is virtually unknown. We conducted a comparative analysis on a global scale to test whether the diversity of human diseases, some of them responsible for high incidences of morbidity and mortality, were associated with host life-history characteristics. After controlling for direct confounding effects exerted by historical, spatial, economic, and population patterns and their interactions, our findings show that human fertility increases with the diversity and structure of disease types. Thus, disease control may not only lower the costs associated with morbidity, but could also contribute directly or indirectly to reductions in human population growth.

Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp.

Wolbachia are bacteria that live in the cells of various invertebrate species to which they cause a wide range of effects on physiology and reproduction. We investigated the effect of Wolbachia infection in the parasitic wasp, Asobara tabida Nees (Hymenoptera, Braconidae). In the 13 populations tested, all individuals proved to be infected by Wolbachia. The removal of Wolbachia by antibiotic treatment had a totally unexpected effect-aposymbiotic female wasps were completely incapable of producing mature oocytes and therefore could not reproduce. In contrast, oogenesis was not affected in treated Asobara citri, a closely related species that does not harbor Wolbachia. No difference between natural symbiotic and cured individuals was found for other adult traits including male fertility, locomotor activity, and size, indicating that the effect on oogenesis is highly specific. We argue that indirect effects of the treatments used in our study (antibiotic toxicity or production of toxic agents) are very unlikely to explain the sterility of females, and we present results showing a direct relationship between oocyte production and Wolbachia density in females. We conclude that Wolbachia is necessary for oogenesis in these A. tabida strains, and this association would seem to be the first example of a transition from facultative to obligatory symbiosis in arthropod-Wolbachia associations.

Antagonistic coevolution over productivity gradients.

This study addresses the question of how spatial heterogeneity in prey productivity and migration act to determine geographic patterns in antagonistic coevolution with a predator. We develop and analyze a quantitative coevolutionary model for a predator-prey interaction. If the model is modified appropriately, the results could broadly apply to multispecies communities and to herbivore-plant, parasite-host, and parasitoid-host associations. Model populations are distributed over a gradient in prey birth rate (as a measure of productivity). Each population, in each patch, is made up of a suite of strains. Each strain of the predator has a certain ability to successfully attack each strain of the prey. We consider scenarios of isolated patches, global migration, and stepping-stone (i.e., local) migration over a linear string of patches. The most pervasive patterns are the following: investments in predator offense and prey defense are both maximal in the patches of highest prey productivity; when there are no constraints on maximal investment, mean predation evolves to highest levels in the most productive patches; similarly, the predator has a greater impact (measured as the percentage reduction in prey density) on the prey population in high productivity patches as compared with low productivity ones-in spite (even after evolution) of prey abundance being highest in the most productive patches; and migration has the net effect of shunting relatively offensive and defensive strains from productive patches to nonproductive ones, potentially resulting in the elimination of otherwise rare, low-investment clones. A modification of the model to gene-for-gene type interactions predicts that generalist strains (in terms of the range of strains the predator can exploit or the prey can fend off) dominate in productive areas of the prey, whereas specialists prevail in marginal habitats. Assuming a wide range of productivities over the prey's geographical distribution, the greatest strain diversity should be found in habitats of intermediate productivity. We discuss the implications of our study for adaptation and conservation. Empirical studies are in broad accord with our findings.

Parasitic effects on host life-history traits: a review of recent studies.

We review empirical studies bearing on the effects of parasites on the age of maturity of their hosts. The few cases already published support theoretical predictions, namely a decrease of host prereproductive life-span unless parasites are benign. Host responses may be due either to phenotypic plasticity or to genetic differences, and even though very few studies on this topic have already been published both mechanisms occur. Promising areas of research include the distribution of age-specific potential costs of resistance to parasitism, as well as the evolution of age-specific parasite preferences under the concomitant evolution of host life-history traits.

Refuge theory and biological control.

An important question in ecology is the extent to which populations and communities are governed by general rules. Recent developments in population dynamics theory have shown that hosts' refuges from their insect parasitoids predict parasitoid community richness patterns. Here, the refuge theory is extended to biological control, in which parasitoids are imported for the control of insect pests. Theory predicts, and data confirm, that the success of biological control is inversely related to the proportion of insects protected from parasitoid attack. Refuges therefore provide a general mechanism for interpreting ecological patterns at both the community level (their species diversity) and population level (their dynamics).

Refuges as a predictor of parasitoid diversity.

A central problem in ecology is predicting the diversity of communities. Insect parasitoids may encompass 20 percent of all insect species; hence, establishing the mechanisms that drive parasitoid species richness represents a major step in understanding the diversity of terrestrial communities. An assemblage model, based on population dynamic constructs, shows how the presence of refuges from parasitoid attack can generate diversity patterns that are in good accord with global data on structural protection from parasitism resulting from host feeding biology. This theory offers a simple ecological explanation for the range of diversities observed in real parasitoid assemblages. Predicting parasitoid diversity may be a realistic goal, at least for those systems in which the basic demography is well understood.

Non-linear transmission rates and the dynamics of infectious disease.

This study considers how non-linearities in the transmission of microparasitic infections affect the population dynamics of host-parasite systems in which the disease is potentially lethal to the host. Non-linearities can either lead to a locally stable or unstable host-parasite equilibrium point, depending on the respective contributions of healthy and infected hosts to the functional form of the transmission rate. Analysis of the non-linear transmission model results in a revealing pair of local stability criteria. Specifically, stability requires sufficient total levels of intrinsic growth of the host population and total levels of density-dependent transmission. The most stable systems occur when increases in the density of healthy hosts result in increases in transmission efficiency, and increases in the number of infected hosts result in small decreases in transmission efficiency. These appear to be very reasonable relationships for directly transmitted microparasites.

Competition between kingdoms.

Although studies of interspecific competition have traditionally been concerned with interactions between closely related species, ecological systems teem with examples of competition between representatives not only from different phyla, but even from different kingdoms. Indeed, inter-kingdom competition may be one of the commonest forms of interaction in nature; particularly prevalent are competitive interactions for shared hosts between insect parasitoids and pathogens from four other kingdoms. Ecologists have barely started to explore the ecological and evolutionary implications of interkingdom competition.

The potential role of pathogens in biological control.

It is now well established that pathogens such as viruses, fungi bacteria and protozoans can have profound effects on the dynamics of their invertebrate host populations. Theoretical models of invertebrate host-pathogen interactions which assume uniform structure of the pathogen population may reasonably explain the oscillatory behaviour observed in some systems, but do not adequately describe the existence of more constant populations found in other host-pathogen interactions. An examination of the literature relating to these relatively stable systems suggests that the common thread is the eventual transmission of some of the more protected, longer-lived stages of the pathogen occurring in reservoirs, such as the soil, host cadavers on trees, or the live host itself. In this letter, I propose a new theoretical model which incorporates this population structure and accounts for the range of dynamics observed in natural systems. In particular, I show that host populations may be regulated to low and relatively constant densities if sufficient numbers of pathogens are trans-located from pathogen reservoirs to habitats where transmission can occur. An understanding of pathogen reservoirs may be of value in the design of biological control programmes and may greatly increase the effectiveness of pathogens as biological control agents.