Author sequence and credit for contributions in multiauthored publications.
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Authorship↗
Biomedical subjects
Michael E Hochberg
Publications and source records attributed to Michael E Hochberg.
Coevolution of symbiotic mutualists and parasites in a community context.
Recent advances in our knowledge of parasitic and mutualistic associations have confirmed the central role of coevolutionary interactions in population and community ecology. Here, we discuss the potential coevolutionary interdependence of the strength and specificity of symbiotic interactions with the complexity and productivity of their environment. We predict that interactions become less beneficial with increasing environmental quality and that the association of productivity with symbiont specificity depends on the relative strengths of tradeoffs between host range and other life-history parameters. However, as biotic complexity increases, pathogen specificity is predicted to decline, whereas mutualist specificity will increase. Testing these predictions on a geographical scale would contribute significantly to the predictive science of coevolution, and to our ability to manage biological interactions embedded in increasingly fragmented landscapes.
Animals↗
Character displacement promotes cooperation in bacterial biofilms.
Resource competition within a group of cooperators is expected to decrease selection for cooperative behavior but can also result in diversifying selection for the use of different resources, which in turn could retard the breakdown of cooperation. Diverse groups are likely to be less susceptible to invasion by noncooperating social cheats: First, competition repression resulting from character displacement may provide less of a selective advantage to cheating; second, cheats may trade off the ability to exploit cooperators that specialize in one type of resource against cooperators that specialize in another ; third, diverse communities of any kind may have higher invasion resistance because there are fewer resources available for an invader to use . Furthermore, diverse groups are likely to be more productive than clonal groups if a wider range of total resources are being used . We addressed these issues by using the cooperative trait of biofilm formation in Pseudomonas fluorescens. Character displacement through resource competition evolved within biofilms; productivity increased with increasing character displacement, and diverse biofilms were less susceptible to invasion by cheats. These results demonstrate that diversification into different ecological niches can minimize selection against cooperation in the face of local resource competition.
Biofilms↗
Fees or refuges: which is better for the sustainable management of insect resistance to transgenic Bt corn?
The evolution of resistance in insect pests will imperil the efficiency of transgenic insect-resistant crops. The currently advised strategy to delay resistance evolution is to plant non-toxic crops (refuges) in close proximity to plants engineered to express the toxic protein of the bacterium Bacillus thuringiensis (Bt). We seek answers to the question of how to induce growers to plant non-toxic crops. A first strategy, applied in the United States, is to require Bt growers to plant non-Bt refuges and control their compliance with requirements. We suggest that an alternative strategy is to make Bt seed more expensive by instituting a user fee, and we compare both strategies by integrating economic processes into a spatially explicit, population genetics model. Our results indicate that although both strategies may allow the sustainable management of the common pool of Bt-susceptibility alleles in pest populations, for the European corn borer (Ostrinia nubilalis) one of the most serious pests in the US corn belt, the fee strategy is less efficient than refuge requirements.
Animals↗
Self-recognition, color signals, and cycles of greenbeard mutualism and altruism.
Altruism presents a challenge to evolutionary theory because selection should favor selfish over caring strategies. Greenbeard altruism resolves this paradox by allowing cooperators to identify individuals carrying similar alleles producing a form of genic selection. In side-blotched lizards, genetically similar but unrelated blue male morphs settle on adjacent territories and cooperate. Here we show that payoffs of cooperation depend on asymmetric costs of orange neighbors. One blue male experiences low fitness and buffers his unrelated partner from aggressive orange males despite the potential benefits of defection. We show that recognition behavior is highly heritable in nature, and we map genetic factors underlying color and self-recognition behavior of genetic similarity in both sexes. Recognition and cooperation arise from genome-wide factors based on our mapping study of the location of genes responsible for self-recognition behavior, recognition of blue color, and the color locus. Our results provide an example of greenbeard interactions in a vertebrate that are typified by cycles of greenbeard mutualism interspersed with phases of transient true altruism. Such cycles provide a mechanism encouraging the origin and stability of true altruism.
Altruism↗
Antagonistic coevolution with parasites increases the cost of host deleterious mutations.
The fitness consequences of deleterious mutations are sometimes greater when individuals are parasitized, hence parasites may result in the more rapid purging of deleterious mutations from host populations. The significance of host deleterious mutations when hosts and parasites antagonistically coevolve (reciprocal evolution of host resistance and parasite infectivity) has not previously been experimentally investigated. We addressed this by coevolving the bacterium Pseudomonas fluorescens and a parasitic bacteriophage in laboratory microcosms, using bacteria with high and low mutation loads. Directional coevolution between bacterial resistance and phage infectivity occurred in all populations. Bacterial population fitness, as measured by competition experiments with ancestral genotypes in the absence of phage, declined with time spent coevolving. However, this decline was significantly more rapid in bacteria with high mutation loads, suggesting the cost of bacterial resistance to phage was greater in the presence of deleterious mutations (synergistic epistasis). As such, resistance to phage was more costly to evolve in the presence of a high mutation load. Consistent with these data, bacteria with high mutation loads underwent less rapid directional coevolution with their phage populations, and showed lower levels of resistance to their coevolving phage populations. These data suggest that coevolution with parasites increases the rate at which deleterious mutations are purged from host populations.
Directed Molecular Evolution↗
Avoid, attack or do both? Behavioral and physiological adaptations in natural enemies faced with novel hosts.
BACKGROUND: Confronted with well-defended, novel hosts, should an enemy invest in avoidance of these hosts (behavioral adaptation), neutralization of the defensive innovation (physiological adaptation) or both? Although simultaneous investment in both adaptations may first appear to be redundant, several empirical studies have suggested a reinforcement of physiological resistance to host defenses with additional avoidance behaviors. To explain this paradox, we develop a mathematical model describing the joint evolution of behavioral and physiological adaptations on the part of natural enemies to their host defenses. Our specific goals are (i) to derive the conditions that may favor the simultaneous investment in avoidance and physiological resistance and (ii) to study the factors that govern the relative investment in each adaptation mode. RESULTS: Our results show that (i) a simultaneous investment may be optimal if the fitness costs of the adaptive traits are accelerating and the probability of encountering defended hosts is low. When (i) holds, we find that (ii) the more that defended hosts are rare and/or spatially aggregated, the more behavioral adaptation is favored. CONCLUSION: Despite their interference, physiological resistance to host defensive innovations and avoidance of these same defenses are two strategies in which it may be optimal for an enemy to invest in simultaneously. The relative allocation to each strategy greatly depends on host spatial structure. We discuss the implications of our findings for the management of invasive plant species and the management of pest resistance to new crop protectants or varieties.
Adaptation, Biological↗
Virulence evolution in emerging infectious diseases.
Models of virulence evolution generally consider the outcome of competition between resident and mutant parasite strains at or near endemic equilibrium. Less studied is what happens during the initial phases of invasion and adaptation. Understanding initial adaptive dynamics is particularly important in the context of emerging diseases in wildlife and humans, for which rapid and accurate intervention may be of the essence. To address the question of virulence evolution in emerging diseases, we employ a simple stochastic modeling framework. As is intuitive, the pathogen strains most likely to emerge are those with the highest net reproductive rates (R0). We find, however, that stochastic events shape the properties of emerging pathogens in sometimes unexpected ways. First, the mean virulence of emerging pathogens is expected to be larger in dense host populations and/or when transmission is high, due to less restrictive conditions for the spread of the pathogen. Second, a positive correlation between average virulence and transmissibility emerges due to a combination of drift and selection. We conclude that at least in the initial phases of adaptation, special assumptions about constraints need not be invoked to explain some virulence-transmission correlations and that virulence management practices should consider how residual variation in transmission and virulence can be selected to reduce the prevalence and/or virulence of emerging infectious diseases.
Biological Evolution↗
The joint evolution of defence and inducibility against natural enemies.
We develop and analyse a model of inducible defence where two traits--defence and its inducibility--jointly evolve. Inducibility reduces costs of defence in the absence of enemies thereby permitting higher defence levels when attacked. If the cost of inducibility is low, then inducibility and defence may reinforce one another, resulting in a runaway leading to a highly inducible and highly effective defence. When inducibility is more costly, a new joint-equilibrium in defence/inducibility emerges displaying intermediate levels of both traits, and the prior 'run-away' scenario (high defence, high inducibility) may disappear. In contrast to the cost of inducibility, the cost of defence has mixed effects. An increase in costs of defence generally diminishes the level of both defence and inducibility at the intermediate locally stable equilibrium, but can favour the existence of the 'run-away' scenario of high defence-high inducibility. The enemy encounter-rate also has mixed effects. At high encounter rates an increase in encounters can lead to a higher/maximal defence and a lower level of inducibility (defence being almost always useful), but at low rates, an increase in encounters can lead to both higher defence and higher inducibility. We finally consider potential enemy responses to defensive change, and illustrate that herd immunity (reduction of encounter rates due to population-level defence) can affect both individual defence and induction that can be, depending on conditions, increased or decreased.
Animals↗
A theory of modern cultural shifts and meltdowns.
Many cultural attributes such as adornment, language slang, mannerisms and rituals are thought to have little or no influence on individual survival and reproduction, functioning rather as markers of cultural identity that promote group cohesion. Here, I show that if cultural markers are under weak selection and subject to loss or substitution, then the breakdown of cultural cohesiveness may proceed without stabilizing reactions until many or most of a culture's identifiers are forever lost. This may culminate in a 'cultural meltdown', whereby the culture is caught in a vortex of ever-decreasing membership and insufficient selection against the accumulation of unfamiliar markers. In progressively altering the topology of communication from diffusion to broadcasting, globalization may be both accelerating the erosion of cultural identities and amplifying dominance behaviours above their normal adaptive levels.
Communication↗
Ecology drives the worldwide distribution of human diseases.
Identifying the factors underlying the origin and maintenance of the latitudinal diversity gradient is a central problem in ecology, but no consensus has emerged on which processes might generate this broad pattern. Interestingly, the vast majority of studies exploring the gradient have focused on free-living organisms, ignoring parasitic and infectious disease (PID) species. Here, we address the influence of environmental factors on the biological diversity of human pathogens and their global spatial organization. Using generalized linear multivariate models and Monte Carlo simulations, we conducted a series of comparative analyses to test the hypothesis that human PIDs exhibit the same global patterns of distribution as other taxonomic groups. We found a significant negative relationship between latitude and PID species richness, and a nested spatial organization, i.e., the accumulation of PID species with latitude, over large spatial scales. Additionally, our results show that climatic factors are of primary importance in explaining the link between latitude and the spatial pattern of human pathogens. Based on our findings, we propose that the global latitudinal species diversity gradient might be generated in large part by biotic interactions, providing strong support for the idea that current estimates of species diversity are substantially underestimated. When parasites and pathogens are included, estimates of total species diversity may increase by more than an order of magnitude.
Biodiversity↗
Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa).
The inevitable escape of transgenic pollen from cultivated fields will lead to the emergence of transgenic crop-wild plant hybrids in natural patches of wild plants. The fate of these hybrids and that of the transgene depend on their ability to compete with their wild relatives. Here we study ecological factors that may enhance the fitness of genetically modified hybrids relative to wild plants for a Bacillus thuringiensis ( Bt) transgene conferring resistance to insects. Mixed stands of wild plants and first-generation hybrids were grown under different conditions of herbivore pressure and density, with Bt oilseed rape ( Brassica napus) as the crop and B. rapa as the wild recipient. Biomass and fitness components were measured from plant germination to the germination of their offspring. The frequency of transgenic seedlings in the offspring generation was estimated using the green fluorescent protein marker. The biomass of F(1) Bt-transgenic hybrids relative to that of wild-type plants was found to be sensitive to both plant density and herbivore pressure, but herbivore pressure appeared as the major factor enhancing their relative fitnesses. In the absence of herbivore pressure, Bt hybrids produced 6.2-fold fewer seeds than their wild neighbors, and Bt plant frequency fell from 50% to 16% within a single generation. Under high herbivore pressure, Bt hybrids produced 1.4-fold more seeds, and Bt plant frequency was 42% in the offspring generation. We conclude that high-density patches of highly damaged wild plants are the most vulnerable to Bt-transgene invasion. They should be monitored early to detect potential transgene spread.
Bacillus thuringiensis↗
Socially mediated speciation.
We employ a simple model to show that social selection can lead to prezygotic reproductive isolation. The evolution of social discrimination causes the congealing of phenotypically similar individuals into different, spatially distinct tribes. However, tribal formation is only obtained for certain types of social behavior: altruistic and selfish acts can produce tribes, whereas spiteful and mutualistic behaviors never do. Moreover, reduced hybrid fitness at tribal borders leads to the selection of mating preferences, which then spread to the core areas of the respective tribes. Unlike models of resource competition, our model generates reproductive isolation in an ecologically homogeneous environment. We elaborate on how altruistic acts can lead to reproductive isolation, but also predict that certain types of competition can lead to the speciation effect. Our theory provides a framework for how individual-level interactions mold lineage diversification, with parapatric speciation as a possible end product.
Social Behavior↗
Does multiple infection select for raised virulence?
Classical models of virulence evolution conclude that the increased competition favoured by multiple infection will select for increasing consumption and deterioration of the host resource, or 'virulence'. However, recent empirical and theoretical studies suggest that this view of virulence has some shortcomings. Here, we argue that the evolutionary consequences of multiple infection depend critically on whether the exploitation rate of an individual parasite is governed directly by the behaviour of the individual, or whether it is limited by the collective behaviour of the coinfecting group. We illustrate that, depending on the mechanistic details of exploitation, multiple infection can select for reduced virulence.
Biological Evolution↗
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.
antagonism↗