Microbially assisted rescue of host populations

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Abstract

Rapid environmental change can drive populations into decline but host genomes may adapt in time to rescue the population from extinction. Host-associated microbes may alter this race. We here develop a population-genetics model to characterize the dynamics and consequences of microbe-assisted host population rescue. In our model, we replace one locus of a classical two-locus system with microbial carriage. Under weak selection the microbial variables settle to a quasi-microbial equilibrium (QME) conditional on the host allele, reducing the coupled dynamics to host allele frequency and abundance. The reduction identifies two microbial contributions that shape rescue. Additive benefits of microbial carriage on host fitness raise host growth immediately without affecting evolution and lift the floor of the demographic rescue-U. By contrast, positive interactions between the rescue allele and the microbe accelerate evolution and narrow the rescue-U instead of buffering initial decline. A microbe can therefore buy time, speed adaptation, or be required for recovery when neither contribution suffices alone. Imperfect microbial inheritance, however, can impede microbe-assisted rescue. When selection acts through fecundity and carriers transmit the microbe to only some offspring, adaptation generates non-carrying descendants faster than transmission replaces them. When that loss is sufficiently strong, recovery can fail even though the allele, the microbe, and their interaction are each individually beneficial. We call this selection-amplified dilution. Together, our model integrates evolutionary rescue theory with multilocus population genetics and evolutionary epidemiology to define a framework of microbe-assisted host rescue, thereby identifying key factors driving or compromising the rescue process.

Significance

Microbes living in and on animals and plants influence key components of host fitness, raising the question of whether they can determine if a population survives severe environmental change. We here develop a mathematical model that separates two ways they do it. A microbe can raise host growth directly, cushioning the population while its genes catch up, or it can influence how strongly a beneficial host gene is favored, speeding up evolutionary adaptation. The model additionally reveals an unexpected failure mode: when successful hosts pass the microbe to only some of their offspring, adaptation itself can erode a beneficial microbe enough to prevent recovery. Overall, our model identifies distinct mechanisms and their signatures of how associated microbes can enhance evolutionary rescue of their hosts.

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