The evolution of mutation rate in an antagonistic coevolutionary model with maternal transmission of parasites

Abstract

By constantly selecting for novel genotypes, coevolution between hosts and parasites can favour elevated mutation rates. Models of this process typically assume random encounters. However, offspring are often more likely to encounter their mother's parasites. Because parents and offspring are genetically similar, they may be susceptible to the same parasite strains and thus, in hosts, maternal transmission should select for mechanisms that decrease intergenerational genetic similarity. In parasites, however, maternal transmission should select for genetic similarity. We develop and analyse a model of host and parasite mutation rate evolution when parasites are maternally inherited. In hosts, we find that maternal transmission has two opposing effects. First, it eliminates coevolutionary cycles that previous work shows select for higher mutation. Second, it independently selects for higher mutation rates, because offspring that differ from their mothers are more likely to avoid infection. In parasites, however, the two effects of maternal transmission act in the same direction. As for hosts, maternal transmission eliminates coevolutionary cycles, thereby reducing selection for increased mutation. Unlike for hosts, however, maternal transmission additionally selects against higher mutation by favouring parasite offspring that are the same as their mothers.

Parasite transmission among relatives halts Red Queen dynamics

“…With stronger selection (such as with higher levels of virulence), the minimum strength of familial transmission needed to eliminate cycles is somewhat higher, but still surprisingly small. This result is consistent with what was found by Greenspoon and M'Gonigle (2013), who studied a mixed vertical and horizontal transmission matching-matching alleles system (see their Fig. 2A).…”

“…Here, we present one‐ and two‐locus models in which a host individual can be infected either by a parasite strain infecting a genotypically similar host, or from a strain infecting a randomly selected host. This differs from a mixed vertical and horizontal transmission model (e.g., Greenspoon and M'Gonigle ) because our model permits preferential transmission from any genetically similar individuals in the previous generation, not only transmission from mother to offspring (vertical transmission). Besides adding generality to the model, this also has the added advantage of simplifying the model, and permitting an analytical understanding of cycles, which was not possible in the model of Greenspoon and M'Gonigle ().…”

“…This differs from a mixed vertical and horizontal transmission model (e.g., Greenspoon and M'Gonigle ) because our model permits preferential transmission from any genetically similar individuals in the previous generation, not only transmission from mother to offspring (vertical transmission). Besides adding generality to the model, this also has the added advantage of simplifying the model, and permitting an analytical understanding of cycles, which was not possible in the model of Greenspoon and M'Gonigle (). Unlike the previous study, we also consider systems with two loci and fluctuating LD, more than two alleles per locus, and an inverse‐matching alleles model in addition to a matching‐alleles model.…”

Host-parasite interactions and the evolution of nonrandom mating

“…This approach allows us to investigate nonrandom parasite transmission. Similar approaches have been used to evaluate the effect of maternal transmission on the evolution of sex (Agrawal ) and the evolution of mutation rate (Greenspoon and M'Gonigle ).…”

“…). Recent theoretical work has shown that maternal transmission of parasites changes predictions about the evolution of sex (Agrawal ) and mutation rate (Greenspoon and M'Gonigle ). Maternally transmitted parasites tend to be genetically well targeted to offspring by virtue of the genetic similarity between mother and offspring.…”