Reproductive parasitism: maternally inherited symbionts in a biparental world

Abstract

Most species of insect, and many other plants and animals, carry maternally heritable microorganisms-viruses, bacteria, unicellular eukaryotes, and fungi that pass from a female host to her progeny. Maternal inheritance establishes a correlation between the fitness of symbiont and host female, which can select for the symbiont to contribute to host fitness. Nevertheless, its lack of transmission through male hosts places the symbiont in conflict with biparentally inherited nuclear genes. In this review, we first examine how this conflict is manifest in selection to promote the production and survival of infected female hosts and gametes. We then examine how the distorted population sex ratios that they produce may affect host reproductive ecology, and thus the intensity of other conflicts associated with sexual reproduction. Finally, we examine evolved host responses to symbiont manipulation. We argue that the unusual intensity of symbiont-host conflict generates extreme selection pressures that can drive changes in sex-determination systems, the basic pathway through which males and females are constructed.

Figure 1.

Equilibrium prevalence of a cost-free maternally inherited male-killing bacterium that is transmitted to a fraction 1 − μ of daughters, and whose daughters have increased chance of survival 1 + b associated with the death of their brothers. Calculated from p* = [(1 − μ)(1 + b) − 1]/b, following, Hurst (1991). Lines represent, from left to right, b = 0.25, b = 0.2, b = 0.15, b = 0.1, b = 0.05, and b = 0.01.

Figure 2.

Cross-compatibility relationships in the presence of Wolbachia/Cardinium inducing CI. (A) Compatibility (viable zygotes) for the case of unidirectional incompatibility (one symbiont)—crosses are compatible save between infected male and uninfected female. (B) Compatibility for bidirectional incompatibility, with two symbionts, W₁ and W₂, alongside uninfected individuals. Wolbachia-infected males are incompatible with both uninfected females and females carrying the alternate strain.