Reproductive Parasitism and Positive Fitness Effects of Heritable Microbes

Abstract

The classification of host–symbiont relationships is usually defined along the parasitism‐mutualism spectrum. It has long been proposed that transmission route is a key factor driving this, with vertical transmission leading to mutualism and horizontal transmission leading to parasitism. However, uniparental vertical transmission can lead to the evolution of reproductive parasitism, whereby host reproduction is skewed to increase the proportion of females within a population or else to reduce the comparative fitness of uninfected females (to the detriment of overall host fitness). Once discussed separately from beneficial effects and mutualism, we now recognise reproductive parasitism is not exclusive of other symbiont phenotypes. We outline the evolution and relationship of reproductive parasitism with respect to positive fitness effects for hosts, and how these interactions may be dynamic across the parasitism‐mutualism continuum.

Key Concepts

  • Exclusive maternal transmission of microbes can create strong selection for reproductive parasitism.
  • Heritable microbes are also selected to confer a range of positive effects on host function and physiology.
  • Where heritable microbes act both as reproductive parasites, and as a positive influence on host function, they are referred to as Jekyll and Hyde symbionts.
  • The presence of positive effects on host function can facilitate the invasion and maintenance of reproductive parasites in host populations.
  • Reproductive parasitism may likewise provide a context in which symbionts may evolve host‐beneficial phenotypes.
  • Symbionts that combine reproductive parasitism with positive effects on host function constitute a useful mechanism for modification of insect host biology in natural populations, coupling a strong gene drive system to a beneficial trait.
  • The presence of multiple phenotypes may aid the spread of heritable microbes through host communities, by enabling host shift events.
  • Lateral transfer of genetic information between microbes can provide the mutational mechanism through which Jekyll and Hyde symbionts arise.

Keywords: reproductive parasite; heritable microbe; vertical transmission; sex ratio distorter; conditional sterility; fitness benefit; cost‐benefit; obligate mutualism; facultative mutualism; uniparental inheritance

Figure 1. Common reproductive manipulation phenotypes expressed by heritable microbes are shown from a–e. All transmission of reproductive parasites (RP) is vertical unless additionally indicated and the proposed adaptive benefits of each phenotype are highlighted in blue. Phenotype (a) is expressed during the host larval stage, killing males and allowing horizontal transmission of the RP to female larvae. (b) shows the differential fate of male and female embryos under embryonic male killing. Infected virgin hosts reproduce via parthenogenesis to produce all female infected broods (c). For phenotype (d) mated infected females produce male and female offspring, but genetic males are converted to functional females. RPs produce mating incompatibilities in (e) for female hosts that are uninfected or carry a different strain, two types are shown.
Figure 2. Possible selection pressures acting on host–symbiont interactions and the effect of symbiont removal on host fitness. Selection acts upon different members of the symbiosis (indicated by coloured arrows: host = yellow, symbiont = green, host and symbiont = blue), leading to the evolution of different situations (arrow terms). In the case of reproductive parasitism, removal of the symbiont will have a positive effect on host fitness (blue area). When other situations have evolved, to mitigate the costs of infection or confer a benefit, then removal of the symbiont can have negative consequences for host fitness (red area).
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Further Reading

Brownlie JC and Johnson KN (2009) Symbiont‐mediated protection in insect hosts. Trends in Microbiology 17: 348–354.

Hurst GDD and Frost CL (2015) Reproductive parasitism: maternally inherited symbionts in a biparental world. Cold Spring Harbour Perspectives in Biology 7: 1–21.

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Zchori‐Fein E and Bourtzis K (2011) Manipulative Tenants: Bacteria Associated with Arthropods, 1st edn. Boca Raton: CRC Press.

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Drew, Georgia C, Frost, Crystal L, and Hurst, Gregory DD(Feb 2019) Reproductive Parasitism and Positive Fitness Effects of Heritable Microbes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028327]