Microbes are potential key players in the evolution of life histories and aging in Caenorhabditis elegans

Abstract

Microbes can have profound effects on host fitness and health and the appearance of late-onset diseases. Host-microbe interactions thus represent a major environmental context for healthy aging of the host and might also mediate trade-offs between life-history traits in the evolution of host senescence. Here, we have used the nematode Caenorhabditis elegans to study how host-microbe interactions may modulate the evolution of life histories and aging. We first characterized the effects of two non-pathogenic and one pathogenic Escherichia coli strains, together with the pathogenic Serratia marcescens DB11 strain, on population growth rates and survival of C. elegans from five different genetic backgrounds. We then focused on an outbred C. elegans population, to understand if microbe-specific effects on the reproductive schedule and in traits such as developmental rate and survival were also expressed in the presence of males and standing genetic variation, which could be relevant for the evolution of C. elegans and other nematode species in nature. Our results show that host-microbe interactions have a substantial host-genotype-dependent impact on the reproductive aging and survival of the nematode host. Although both pathogenic bacteria reduced host survival in comparison with benign strains, they differed in how they affected other host traits. Host fertility and population growth rate were affected by S. marcescens DB11 only during early adulthood, whereas this occurred at later ages with the pathogenic E. coli IAI1. In both cases, these effects were largely dependent on the host genotypes. Given such microbe-specific genotypic differences in host life history, we predict that the evolution of reproductive schedules and senescence might be critically contingent on host-microbe interactions in nature.

Keywords: C. elegans; aging; host–microbe interactions; life‐history evolution; microbes; trade‐offs.

FIGURE 1

Genotype‐by‐environment (bacteria) interactions affect Caenorhabditis elegans population growth and survival. In (a), population growth rates of the five C. elegans genotypes, measured at the early (72 h) and delayed reproduction (114 h) times, reveal bacterial‐specific effects on the temporal dynamics of reproductive output (significant three‐way interaction, p‐value < .001). In (b), it is shown that mean lifespan also depends on the interaction between C. elegans genotype and bacterial strain. Letters above symbols indicate group assignment from significant post hoc tests (p‐value < .05) obtained with data for each bacteria independently. Mean estimates and SE are shown in (a) and predicted values are shown in (b). Note the logarithmic scale of the y axis in (a).

FIGURE 2

Bacterial‐specific effects on the reproductive output and survival are maintained in the genetically diverse, male–female, Caenorhabditis elegans host population. As in Figure 1, (a) shows population growth rates measured at the early (72 h) and delayed reproduction (114 h) times, with each of the four bacteria used in this study. In (b), mean lifespan reveals the detrimental effects of the pathogenic Escherichia coli IAI1 and Serratia marcescens Db11 bacteria in contrast with the benign E. coli HT115(DE3) and E. coli OP50 strains. Letters above symbols indicate group assignment from significant post hoc tests (p‐value < .05). In (a) and (b) mean estimates and SE are shown.

FIGURE 3

Bacteria affect the reproductive schedule and developmental rate of the genetically diverse, male–female, Caenorhabditis elegans D00 host population. (a) shows the lifetime reproductive success in the presence of the four different bacteria, while (b) shows the reproductive schedule. The age at first reproduction (AFR), given in hours and days after L1 seed (for comparison with other panels in the figure) is displayed in the dot plot in (c). In (d), the percentage of adult females and males at day 3 is given for the D00 population with the same bacteria. Note that, for the results shown in panels (a), (b), and (c), females were crossed with males that were one day older (see Section 2). Means and SE are provided. Letters above bars indicate group assignment based on post hoc tests (adjusted p‐value < .05, see Section 2), which in (b) were performed within each time period.