Some symbiotic associations are nasty, and some are nice – why is there so much variation in interspecific interactions?
One idea is that competition between parasite genotypes can select for higher virulence (Frank 1996). When different parasite strains or species infect the same host, they may compete for host resources. The more competitive genotype will win out, producing more transmissible stages. This genotype’s competitive ability may also correspond to elevated virulence – it is more competitive because it can exploit its host more rapidly and aggressively. If hosts are commonly infected with multiple parasite genotypes, we’d then predict the evolution of higher virulence in the parasite population.
I assisted Manuela López-Villavicencio, Tatiana Giraud and many others in an experimental test of this hypothesis. We found that the virulence of the fungus Microbotryum violaceum, the agent of anther-smut, is elevated when multiple strains infect its host Silene latifolia. This elevated virulence seems to result from an increase in the growth and reproduction of fungal strains in the presence of competitors, in particular unrelated ones. This aggressive growth results in more sterilization of the host and more transmissible stages (spores) produced by the parasite ( López-Villavicencio et al. 2010 Evolution).
I explored a similar question in the protozoal parasites Toxoplasma gondii and Sarcocystis neurona. These are terrestrial parasites – T. gondii‘s definitive hosts are felines (like house cats) and S. neurona‘s definitive hosts are opossums. However, both can infect a wide range of intermediate hosts. With land-to-sea runoff, this range increasingly includes marine mammals like harbor porpoises and seals. We surveyed a sample of marine mammals that stranded on beaches in the Pacific Northwest and found high rates of protozoal parasitism. Nearly half of infected individuals were infected with both T. gondii and S. neurona, and these cases were associated with more severe disease (Gibson et al. 2011 PLoS NTD). This study calls for additional work to determine if dual infections select for more virulent strains.
Lots of experimental evolution studies show that the transmission of a parasite from mother to offspring (vertical) can select for reduced virulence, while horizontal transmission selects for increased virulence (e.g. Bull et al. 1991; Turner et al. 1998; Stewart et al. 2005). Under horizontal transmission, parasites continually shift between host lineages. There is little potential for coevolution. Under vertical transmission, a parasite and host lineage are paired for multiple generations. Tight coevolution is likely. Thus the potential for coevolution also varies with transmission mode. Does coevolution contribute to the evolution of reduced virulence?
We tested this hypothesis with experimental coevolution of the nematode Caenorhabditis elegans and its lethal bacterial parasite Serratia marcescens. Evolutionary transitions in virulence are relevant to this association. S. marcescens strains vary substantially in virulence to C. elegans. Serratia species are also cuticular or gut mutualists to rhabditid nematodes, including caenorhabditids. We manipulated the potential for coevolution while selecting for reduced antagonism between C. elegans and S. marcescens. We use the term “antagonism” here to emphasize the joint nature of the phenotypes of interest. Though virulence is not exclusively a parasite trait, it is commonly assumed to be.
Our results demonstrate that coevolution contributes to the evolution of reduced antagonism (i.e. reduced virulence). After 20 generations of selection, reduced antagonism evolved only when coevolution was possible. Independent selection on either partner failed to produce evolutionary change. Potentially coevolving lines were strongly locally adapted for reduced antagonism, further underlining the significance of coevolution (Gibson et al. 2015 Evolution).
Infection of C. elegans with S. marcescens. Microscopy and photography help from Erik Ragsdale.
- Bull, J. J., I. J. Molineux, and W. R. Rice. 1991. Selection of benevolence in a host-parasite system. Evolution 45:875-882.
- Frank, S. A. 1996. Models of parasite virulence. Quart Rev Biol 71:37-78.
- Stewart, A. D., J. M. Logsdon, and S. E. Kelley. 2005. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59:730-739.
- Turner, P. E., V. S. Cooper, and R. E. Lenski. 1998. Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52:315-329.