The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

Ecological histories determine the success of social exploitation.

Ecological context often modifies biotic interactions, yet effects of ecological history are poorly understood. In experiments with the bacterium Myxococcus xanthus , resource-level histories of genotypes interacting during cooperative multicellular development were found to strongly regulate social fitness. Yet how developmental spore production responded to variation in resource-level histories between interactants differed greatly between cooperators and cheaters; relative-fitness advantages gained by cheating after high-resource growth were generally reduced or absent if one or both parties experienced low-resource growth. Low-resource growth also eliminated facultative exploitation in some pairwise mixes of cooperation-proficient natural isolates that occurs when both strains have grown under resource abundance. Our results contrast with previous studies in which cooperator fitness correlated positively with resource level and suggest that resource-level variation may be important in regulating whether exploitation of cooperators occurs in a natural context.

Allopatric divergence of cooperators confers cheating resistance and limits effects of a defector mutation.

BACKGROUND: Social defectors may meet diverse cooperators. Genotype-by-genotype interactions may constrain the ranges of cooperators upon which particular defectors can cheat, limiting cheater spread. Upon starvation, the soil bacterium Myxococcus xanthus cooperatively develops into spore-bearing fruiting bodies, using a complex regulatory network and several intercellular signals. Some strains (cheaters) are unable to sporulate effectively in pure culture due to mutations that reduce signal production but can exploit and outcompete cooperators within mixed groups. RESULTS: In this study, interactions between a cheater disrupted at the signaling gene csgA and allopatrically diversified cooperators reveal a very small cheating range. Expectedly, the cheater failed to cheat on all natural-isolate cooperators owing to non-cheater-specific antagonisms. Surprisingly, some lab-evolved cooperators had already exited the csgA mutant's cheating range after accumulating fewer than 20 mutations and without experiencing cheating during evolution. Cooperators might also diversify in the potential for a mutation to reduce expression of a cooperative trait or generate a cheating phenotype. A new csgA mutation constructed in several highly diverged cooperators generated diverse sporulation phenotypes, ranging from a complete defect to no defect, indicating that genetic backgrounds can limit the set of genomes in which a mutation creates a defector. CONCLUSIONS: Our results demonstrate that natural populations may feature geographic mosaics of cooperators that have diversified in their susceptibility to particular cheaters, limiting defectors' cheating ranges and preventing them from spreading. This diversification may also lead to variation in the phenotypes generated by any given cooperation-gene mutation, further decreasing the chance of a cheater emerging which threatens the persistence of cooperation in the system.

Behavioral Interactions between Bacterivorous Nematodes and Predatory Bacteria in a Synthetic Community.

Theory and empirical studies in metazoans predict that apex predators should shape the behavior and ecology of mesopredators and prey at lower trophic levels. Despite the ecological importance of microbial communities, few studies of predatory microbes examine such behavioral res-ponses and the multiplicity of trophic interactions. Here, we sought to assemble a three-level microbial food chain and to test for behavioral interactions between the predatory nematode Caenorhabditis elegans and the predatory social bacterium Myxococcus xanthus when cultured together with two basal prey bacteria that both predators can eat-Escherichia coli and Flavobacterium johnsoniae. We found that >90% of C. elegans worms failed to interact with M. xanthus even when it was the only potential prey species available, whereas most worms were attracted to pure patches of E. coli and F. johnsoniae. In addition, M. xanthus altered nematode predatory behavior on basal prey, repelling C. elegans from two-species patches that would be attractive without M. xanthus, an effect similar to that of C. elegans pathogens. The nematode also influenced the behavior of the bacterial predator: M. xanthus increased its predatory swarming rate in response to C. elegans in a manner dependent both on basal-prey identity and on worm density. Our results suggest that M. xanthus is an unattractive prey for some soil nematodes and is actively avoided when other prey are available. Most broadly, we found that nematode and bacterial predators mutually influence one another's predatory behavior, with likely consequences for coevolution within complex microbial food webs.