Microbial protection favors parasite tolerance and alters host-parasite coevolutionary dynamics

Abstract

Coevolution between hosts and parasites is a major driver of rapid evolutionary change¹ and diversification.^2,3 However, direct antagonistic interactions between hosts and parasites could be disrupted⁴ when host microbiota form a line of defense, a phenomenon widespread across animal and plant species.^5,6 By suppressing parasite infection, protective microbiota could reduce the need for host-based defenses and favor host support for microbiota colonization,⁶ raising the possibility that the microbiota can alter host-parasite coevolutionary patterns and processes.⁷ Here, using an experimental evolution approach, we co-passaged populations of nematode host (Caenorhabditis elegans) and parasites (Staphylococcus aureus) when hosts were colonized (or not) by protective bacteria (Enterococcus faecalis). We found that microbial protection during coevolution resulted in the evolution of host mortality tolerance-higher survival following parasite infection-and in parasites adapting to microbial defenses. Compared to unprotected host-parasite coevolution, the protected treatment was associated with reduced dominance of fluctuating selection dynamics in host populations. No differences in host recombination rate or genetic diversity were detected. Genomic divergence was observed between parasite populations coevolved in protected and unprotected hosts. These findings indicate that protective host microbiota can determine the evolution of host defense strategies and shape host-parasite coevolutionary dynamics.

Keywords: Arms Race; Red Queen; diversity; host-parasite coevolution; microbiota; protective symbiosis; recombination; tolerance.

Figure 1

Design of the coevolution experiment (A) Unprotected and (B) protected treatments. Host, Caenorhabditis elegans; protective bacterium, Enterococcus faecalis; parasite, Staphylococcus aureus.

Figure 2

Host adaptation during unprotected and protected coevolution Evolution of host tolerance strategies against parasite infection. (A) Colony-forming units (CFUs) of ancestral parasites per host across ancestral, unprotected coevolved, and protected coevolved backgrounds (n = 58). Error bars are SEM. (B) Number of eggs per host across host backgrounds during infection with ancestral parasites (n = 52). Error bars are SEM. C) Proportion of live hosts across host backgrounds during ancestral parasite infection (n = 51). Error bars are SEM. (D) CFUs of protective bacteria per host across host backgrounds during ancestral parasite infection (n = 51). Error bars are SEM. (E) Number of eggs from protected hosts across host backgrounds during ancestral parasite infection (n = 20). Error bars are SEM.

Figure 3

Parasite adaptation during unprotected and protected coevolution (A) CFUs of parasites per protected host for each parasite background across pooled host backgrounds (n = 265). Error bars are SEM. (B) CFUs of parasites per μL media grown in in vitro co-culture with protective bacteria (n = 96). Error bars are SEM.

Figure 4

Host genomic evolution during unprotected and protected coevolution (A) Number of alleles under fluctuating (Red Queen) (dark gray bars) or directional (Arms Race) (pale gray bars) selection. (B) Selection coefficients for allele frequency changes in the host for the second (x) and first (y) half of the evolution experiment for the protected treatment. (C) Selection coefficients for allele frequency changes in the host for the second (x) and first (y) half of the evolution experiment for the unprotected treatment. (D) The relationship between recombination rate for a given chromosomal region and the number of alleles under selection for alleles under directional (Arms Race) or fluctuating (Red Queen) selection. Reciprocal analysis for the parasite can be found in Figures S1–S4 and Tables S1, S2, and S3.