Abstract

The fitness effects associated with Wolbachia infection have wide-ranging ecological and evolutionary consequences for host species. How these effects are modulated by the relative influence of host and Wolbachia genomes has been described as a balancing act of genomic cooperation and conflict. For vertically transmitted symbionts, like cytoplasmic Wolbachia, concordant host–symbiont fitness interests would seem to select for genomic cooperation. However, Wolbachia’s ability to manipulate host reproductive systems and distort offspring sex ratios presents an evolutionary conflict of interest with infected hosts. In the parthenogenesis-inducing (PI) form of Wolbachia found in many haplodiploid insects, Wolbachia fitness is realized through females and is enhanced by their feminization of male embryos and subsequent parthenogenetic reproduction. In contrast, as long as Wolbachia is not fixed in a population and sexual reproduction persists, fitness for the host species is realized through both male and female offspring production. How these cooperating and competing interests interact and the relative influence of host and Wolbachia genomes were investigated in the egg parasitoid Trichogramma kaykai, where Wolbachia infection has remained at a low frequency in the field. A factorial design in which laboratory cultures of Wolbachia-infected T. kaykai were cured and re-infected with alternative Wolbachia strains was used to determine the relative influence of host and Wolbachia genomes on host fitness values. Our results suggest fitness variation is largely a function of host genetic background, except in the case of offspring sex ratio where a significant interaction between host and Wolbachia genomes was found. We also find a significant effect associated with the horizontal transfer of Wolbachia strains, which we discuss in terms of the potential for coadaptation in PI-Wolbachia symbioses.

Highlights

  • The alphaproteobacterium Wolbachia pipientis is a widely distributed cytoplasmic symbiont among arthropods and nematodes, and occupies an ecological niche distinguished by manipulation of host reproduction

  • The effects of Wolbachia infections on different aspects of host fitness directly affect the nature of the symbioses between Wolbachia and their hosts: negative fitness effects resulting in host–symbiont conflicts if they enhance Wolbachia fitness; and positive fitness effects resulting in host–symbiont cooperation

  • The ability to manipulate host reproductive systems by sex ratio distortion presents a potential source of conflict between Wolbachia symbionts and their hosts, since the fitness interests of sexually reproducing hosts differ from maternally inherited Wolbachia symbionts regarding offspring sex ratios, with sexual hosts gaining optimum fitness through male and female offspring and Wolbachia gaining optimum fitness through female offspring alone

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Summary

Introduction

The alphaproteobacterium Wolbachia pipientis is a widely distributed cytoplasmic symbiont among arthropods and nematodes, and occupies an ecological niche distinguished by manipulation of host reproduction. For long-term coevolved symbioses theoretical predictions and empirical results suggest selection will favor alignment of fitness interests for maternally inherited symbionts and their female hosts (Turelli, 1994; Herre et al, 1999; Wade & Goodnight, 2006; Weeks et al, 2007). The ability to manipulate host reproductive systems by sex ratio distortion presents a potential source of conflict between Wolbachia symbionts and their hosts, since the fitness interests of sexually reproducing hosts differ from maternally inherited Wolbachia symbionts regarding offspring sex ratios, with sexual hosts gaining optimum fitness through male and female offspring and Wolbachia gaining optimum fitness through female offspring alone

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