Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite

Abstract

The coevolution between hosts and parasites is predicted to have complex evolutionary consequences for both antagonists, often within short time periods. To date, conclusive experimental support for the predictions is available mainly for microbial host systems, but for only a few multicellular host taxa. We here introduce a model system of experimental coevolution that consists of the multicellular nematode host Caenorhabditis elegans and the microbial parasite Bacillus thuringiensis. We demonstrate that 48 host generations of experimental coevolution under controlled laboratory conditions led to multiple changes in both parasite and host. These changes included increases in the traits of direct relevance to the interaction such as parasite virulence (i.e., host killing rate) and host resistance (i.e., the ability to survive pathogens). Importantly, our results provide evidence of reciprocal effects for several other central predictions of the coevolutionary dynamics, including (i) possible adaptation costs (i.e., reductions in traits related to the reproductive rate, measured in the absence of the antagonist), (ii) rapid genetic changes, and (iii) an overall increase in genetic diversity across time. Possible underlying mechanisms for the genetic effects were found to include increased rates of genetic exchange in the parasite and elevated mutation rates in the host. Taken together, our data provide comprehensive experimental evidence of the consequences of host-parasite coevolution, and thus emphasize the pace and complexity of reciprocal adaptations associated with these antagonistic interactions.

Increased responsiveness in feeding behaviour ofCaenorhabditis elegansafter experimental coevolution with its microparasiteBacillus thuringiensis

“…Our analysis also revealed a significant effect of replicate within host-selection regime. This effect is probably a consequence of independent evolutionary trajectories in the replicate populations within the same evolution treatment, as already shown for these populations previously [15,20].…”

“…(b) Feeding behaviour experiment The general experimental conditions were identical to those of the phenotypic assays described in the work of Schulte et al [15]. All nematodes were taken from the replicate populations of the final host generation of the evolution experiment.…”

“…Replicate numbers were not 20 as in the study of Schulte et al [15] since for some replicates the available worm numbers were insufficient to allow tests in both bacterial treatments. Moreover, one of the coevolved populations was excluded from statistical analysis because worms did not feed at all under non-pathogenic conditions, which represents an artefact [10].…”

“…(a) Study system The exact material and protocol for the evolution experiment is described elsewhere [15]. Importantly, to enhance evolutionary responses, we used mixtures of three different BT strains (NRRL B-18246, NRRL B-18247 and NRRL B-18679) in a 5 : 5 : 1 ratio and outcrossed populations of three different natural C. elegans isolates (MY8, MY15 and MY18; [16]).…”

“…We compared feeding rates of nematode populations that coevolved with pathogenic BT strains for about 48 generations with control populations that evolved in the absence of pathogenic strains under otherwise identical conditions [15].…”