Michael E. Hochberg

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.

PREDATORS, PARASITOIDS, AND PATHOGENS AS MORTALITY AGENTS IN PHYTOPHAGOUS INSECT POPULATIONS

We compiled life tables for 78 holometabolous herbivorous insect species to quantify levels of apparent enemy-induced mortality of immature insects. Enemies were classified by type (predator, parasitoid, or pathogen), and mortalities caused by each type in each herbivore immature stage were tested with Analysis of Deviance for differences associated with four ecological characteristics of preadult herbivores: feeding biology, invasion status, and the cultivation status and latitudinal zone of the habitat. Total enemy- induced mortality is higher in the late developmental stages, and overall, parasitoids kill more herbivores than do either predators or pathogens. Among the ecological variables, both feeding biology and latitude showed significant enemy effects in at least one late developmental stage, whereas neither cultivation status nor invasion status was associated with enemy-induced mortality in any stage. Bonferroni adjustment of probabilities for multiple comparisons resulted in few significant interactions between enemy type and the ecological variables. However, raw probabilities and comparisons across herbivore im- mature stages suggest several patterns that deserve attention in future studies: (1) endophytic herbivores suffer lower mortality by predators and pathogens than exophytics, and endo- phytic leaf miners suffer the greatest parasitoid-induced mortality, while endophytic gallers/ borers/root feeders suffer the least; (2) overall enemy-induced mortality is similar in natural and cultivated habitats; (3) exotic insects do not suffer lower enemy-induced mortality rates than natives; and (4) predation and disease may be greater in tropical/subtropical habitats, whereas parasitism is greater in the temperate zone. These results identify several general patterns in insect demographics that should be useful for hypothesis testing.

Hot Spots, Cold Spots, and the Geographic Mosaic Theory of Coevolution

Species interactions commonly coevolve as complex geographic mosaics of populations shaped by differences in local selection and gene flow. We use a haploid matching‐alleles model for coevolution to evaluate how a pair of species coevolves when fitness interactions are reciprocal in some locations (“hot spots”) but not in others (“cold spots”). Our analyses consider mutualistic and antagonistic interspecific interactions and a variety of gene flow patterns between hot and cold spots. We found that hot and cold spots together with gene flow influence coevolutionary dynamics in four important ways. First, hot spots need not be ubiquitous to have a global influence on evolution, although rare hot spots will not have a disproportionate impact unless selection is relatively strong there. Second, asymmetries in gene flow can influence local adaptation, sometimes creating stable equilibria at which species experience minimal fitness in hot spots and maximal fitness in cold spots, or vice versa. Third, asymmetries in gene flow are no more important than asymmetries in population regulation for determining the maintenance of local polymorphisms through coevolution. Fourth, intraspecific allele frequency differences among hot and cold spot populations evolve under some, but not all, conditions. That is, selection mosaics are indeed capable of producing spatially variable coevolutionary outcomes across the landscapes over which species interact. Altogether, our analyses indicate that coevolutionary trajectories can be strongly shaped by the geographic distribution of coevolutionary hot and cold spots, and by the pattern of gene flow among populations.

The evolutionary ecology of metacommunities.

Research on the interactions between evolutionary and ecological dynamics has largely focused on local spatial scales and on relatively simple ecological communities. However, recent work demonstrates that dispersal can drastically alter the interplay between ecological and evolutionary dynamics, often in unexpected ways. We argue that a dispersal-centered synthesis of metacommunity ecology and evolution is necessary to make further progress in this important area of research. We demonstrate that such an approach generates several novel outcomes and substantially enhances understanding of both ecological and evolutionary phenomena in three core research areas at the interface of ecology and evolution.

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 preys 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.

A conceptual framework for the evolution of ecological specialisation

Ecology Letters (2011) 14: 841-851 ABSTRACT: Ecological specialisation concerns all species and underlies many major ecological and evolutionary patterns. Yet its status as a unifying concept is not always appreciated because of its similarity to concepts of the niche, the many levels of biological phenomena to which it applies, and the complexity of the mechanisms influencing it. The evolution of specialisation requires the coupling of constraints on adaptive evolution with covariation of genotype and environmental performance. This covariation itself depends upon organismal properties such as dispersal behaviour and life history and complexity in the environment stemming from factors such as species interactions and spatio-temporal heterogeneity in resources. Here, we develop a view on specialisation that integrates across the range of biological phenomena with the goal of developing a more predictive conceptual framework that specifically accounts for the importance of biotic complexity and coevolutionary events.

Evolutionary rescue: an emerging focus at the intersection between ecology and evolution.

There is concern that the rate of environmental change is now exceeding the capacity of many populations to adapt. Mitigation of biodiversity loss requires science that integrates both ecological and evolutionary responses of populations and communities to rapid environmental change, and can identify the conditions that allow the recovery of declining populations. This special issue focuses on evolutionary rescue (ER), the idea that evolution might occur sufficiently fast to arrest population decline and allow population recovery before extinction ensues. ER emphasizes a shift to a perspective on evolutionary dynamics that focuses on short time-scales, genetic variants of large effects and absolute rather than relative fitness. The contributions in this issue reflect the state of field; the articles address the latest conceptual developments, and report novel theoretical and experimental results. The examples in this issue demonstrate that this burgeoning area of research can inform problems of direct practical concern, such as the conservation of biodiversity, adaptation to climate change and the emergence of infectious disease. The continued development of research on ER will be necessary if we are to understand the extent to which anthropogenic global change will reduce the Earths biodiversity.

THE EVOLUTION OF SPECIFICITY IN EVOLVING AND COEVOLVING ANTAGONISTIC INTERACTIONS BETWEEN A BACTERIA AND ITS PHAGE

Abstract The evolution of exploitative specificity can be influenced by environmental variability in space and time and the intensity of trade-offs. Coevolution, the process of reciprocal adaptation in two or more species, can produce variability in host exploitation and as such potentially drive patterns in host and parasite specificity. We employed the bacterium Pseudomonas fluorescens SBW25 and its DNA phage Φ2 to investigate the role of coevolution in the evolution of phage infectivity range and its relation with phage growth rate. At the phage population level, coevolution led to the evolution of broader infectivity range, but without an associated decrease in phage growth rate relative to the ancestor, whereas phage evolution in the absence of bacterial evolution led to an increased growth rate but no increase in infectivity range. In contrast, both selection regimes led to phage adaptation (in terms of growth rates) to their respective bacterial hosts. At the level of individual phage genotypes, coevolution resulted in within-population diversification in generalist and specialist infectivity range types. This pattern was consistent with a multilocus gene-for-gene interaction, further confirmed by an observed cost of broad infectivity range for individual phage. Moreover, coevolution led to the emergence of bacterial genotype by phage genotype interactions in the reduction of bacterial growth rate by phage. Our study demonstrates that the strong reciprocal selective pressures underlying the process of coevolution lead to the emergence and coexistence of different strategies within populations and to specialization between selective environments.

The ecology of Myrmica ants in relation to the conservation of Maculinea butterflies

Maculinea butterflies in Europe, and probably most of Asia, are host specific social parasites of various species of Myrmica ants. The latest summary of field data showing the pattern of host specificity by Maculinea is presented. Myrmica ants have been well studied in the laboratory but much less is known about the ecology of their natural populations. While the former is important in understanding the adaptive evolution of Maculinea larval behaviours, the latter is of more practical importance to conservationists charged with the protection of specific populations of Maculinea. The current knowledge of habitat partition, colony growth and colony reproduction within communities of Myrmica ants is summarized in relation to the ecology of Maculinea species. Concepts used in current population simulation models are explained. A key concept is the idea that community structure (both number of species and size and abundance of nests) is controlled by the quantity and quality of suitable nest sites. Some advice is given to conservationists who might need to manipulate Myrmica ant populations in order to maintain a robust population of a Maculinea species.

WHEN IS BIOLOGICAL CONTROL EVOLUTIONARILY STABLE (OR IS IT)

The evolution of resistance by insect and weed pests to chemical pesticides is a problem of increasing importance in applied ecology. It is striking that the evolution of resistance by target pest species in biological control is much less frequently reported, particularly in control involving parasitoids and predators, rather than pathogens. Although it is conceivable that this reflects biases in reporting or frequency of application, we suggest that there is a puzzle here worthy of scrutiny, and we outline several potential underlying causes. In order of discussion (not necessarily of importance), these are: (1) lack of genetic variation; (2) genetic constraints on selection; (3) weak selection; (4) temporally varying selection; and (5) coevolutionary dynamics. We, in particular, focus on the potential for weak selection on the host for increased resistance, despite effective control. The very spatial mechanisms (e.g., refuges, metapopulation dynamics) believed to facilitate the per- sistence of many natural enemy-victim systems with strong biological control may also incidentally provide an environment where selection is weak on target pests to evolve improved resistance to control agents, thereby biasing coevolution toward the enemy. The basic insight is that in a spatially heterogeneous environment, a strong limiting factor on a population can be a weak selective factor. The hypotheses presented here provide ingre- dients needed to predict which biological control systems might be evolutionarily stable, and which not. Our aim in this thought piece is to stimulate more attention to the evolu- tionary dimension of biological control systems.