Reproductive Parasitism and Positive Fitness Effects of Heritable Microbes


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).


Beckmann JF , Ronau JA and Hochstrasser M (2017) A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nature Microbiology 2: 1–7.

Brownlie JC , Cass BN , Riegler M , et al. (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathogens 5: e1000368.

Cordaux R , Bouchon D and Grève P (2011) The impact of endosymbionts on the evolution of host sex‐determination mechanisms. Trends in Genetics 27: 332–341.

Cosmides LM and Tooby J (1981) Cytoplasmic inheritance and intergenomic conflict. Journal of Theoretical Biology 89: 83–129.

De Vooght L , Caljon G , Van Hees J , et al. (2015) Paternal transmission of a secondary symbiont during mating in the viviparous tsetse fly. Molecular Biology and Evolution 32: 1977–1980.

Dobson SL , Marsland EJ and Rattanadechakul W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160: 1087–1094.

Duron O (2014) Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. FEMS Microbiol Ecology 90: 184–194.

Elnagdy S , Majerus MEN , Gardener M , et al. (2013) The direct effects of male killer infection on fitness of ladybird hosts (Coleoptera: Coccinellidae). Journal of Evolutionary Biology 26: 1816–1825.

Engelstädter J and Hurst GDD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology, Evolution, and Systematics 40: 127–149.

Fenton A , Johnson KN , Brownlie JC , et al. (2011) Solving the Wolbachia paradox: modeling the tripartite interaction between host, Wolbachia, and a natural enemy. The American Naturalist 178: 333–342.

Fukui T , Kawamoto M , Shoji K , et al. (2015) The endosymbiotic bacterium Wolbachia selectively kills male hosts by targeting the masculinizing gene. PLoS Pathogens 11: 1–14.

Grenier S , Gomes SM , Pintureau B , et al. (2002) Use of tetracycline in larval diet to study the effect of Wolbachia on host fecundity and clarify taxonomic status of Trichogramma species in cured bisexual lines. Journal of Invertebrate Pathology 80: 13–21.

Harumoto T and Lemaitre B (2018) Male‐killing toxin in a bacterial symbiont of Drosophila . Nature 557: 252–255.

Hedges LM , Brownlie JC , O'Neill SL , et al. (2008) Wolbachia and virus protection in insects. Science 322: 702.

Himler AG , Adachi‐Hagimori T , Bergen JE , et al. (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 32: 254–256.

Hoffmann AA , Montgomery BL , Popovici J , et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454–459.

Hornett EA , Charlat S , Duplouy AMR , et al. (2006) Evolution of male‐killer suppression in a natural population. PLoS Biology 4: 1643–1648.

Hosokawa T , Koga R , Kikuchi Y , et al. (2010) Wolbachia as a bacteriocyte‐associated nutritional mutualist. Proceedings of the National Academy of Sciences of the United States of America 107: 769–774.

Huigens ME and Stouthamer R (2003) Parthenogenesis associated with Wolbachia. In: Bourtzis K and Miller TA , Insect Symbiosis, 1nd edn, pp. 247–266. Boca Raton: CRC Press.

Hurst LD (1991) The incidences and evolution of cytoplasmic male killers. Proceedings of the Royal Society of London – Series B 244: 91–99.

Hurst GDD and Majerus MEN (1993) Why do maternally inherited microorganisms kill males? Heredity 71: 81–95.

Jiggins FM , Hurst GDD , Jiggins CD , et al. (2000) The butterfly Danaus chrysippus is infected by a male‐killing Spiroplasma bacterium. Parasitology 120: 439–446.

Kremer N , Voronin D , Charif D , et al. (2009) Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathogens 5: e1000630.

Le Page DP , Metcalf JA , Bordenstein SR , et al. (2017) Prophage WO genes recapitulate and enhance Wolbachia‐induced cytoplasmic incompatibility. Nature 543: 243–247.

Moreira LA , Iturbe‐Ormaetxe I , Jeffery JA , et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and plasmodium. Cell 139: 1268–1278.

Nakanishi K , Hoshino M , Nakai M , et al. (2008) Novel RNA sequences associated with late male killing in Homona magnanima . Proceedings of the Royal Society of London – Series B 275: 1249–1254.

Nikoh N , Hosokawa T , Moriyama M , et al. (2014) Evolutionary origin of insect‐Wolbachia nutritional mutualism. Proceedings of the National Academy of Sciences of the United States of America 111: 10257–10262.

O'Neill SL , Ryan PA , Turley AP , et al. (2018) Scaled deployment of Wolbachia to protect the community from Aedes transmitted arboviruses. Gates Open Research 2: 36.

Paredes JC , Herren JK , Schüpfer F , et al. (2016) The role of lipid competition for endosymbiont‐mediated protection against parasitoid wasps in Drosophila . mBio 7: 1–8.

Teixeira L , Ferreira A and Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLOS Biology 12: 2753–2763.

Turelli M and Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila . Nature 353: 440–442.

Turelli M , Cooper BS , Richardson KM , et al. (2018) Rapid global spread of wRi‐like Wolbachia across multiple Drosophila . Current Biology 28: 963–971.

Unckless RL and Jaenike J (2012) Maintenance of a male‐killing Wolbachia in Drosophila innubila by male‐killing dependent and male‐killing independent mechanisms. Evolution 66: 678–689.

Veneti Z , Zabalou S , Papafotiou G , et al. (2012) Loss of reproductive parasitism following transfer of male‐killing Wolbachia to Drosophila melanogaster and Drosophila simulans . Heredity 109: 306–312.

Walker T , Johnson PH , Moreira LA , et al. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450–455.

Weeks AR , Turelli M , Harcombe WR , et al. (2007) From parasite to mutualist: Rapid evolution of Wolbachia in natural populations of Drosophila . PLoS Biology 5: 0997–1005.

Werren JH (1987) The coevolution of autosomal and cytoplasmic sex ratio factors. Journal of Theoretical Biology 124: 317–334.

Werren JH (1997) Biology of Wolbachia . Annual Review of Entomology 124: 587–609.

Werren JH (2011) Selfish genetic elements, genetic conflict, and evolutionary innovation. Proceedings of the National Academy of Sciences of the United States of America 108: 10863–10870.

Xie J , Butler S , Sanchez G , et al. (2014) Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity 112: 399–408.

Zhang YK , Yang K , Zhu YX , et al. (2018) Symbiont‐conferred reproduction and fitness benefits can favour their host occurrence. Ecology and Evolution 8: 1626–1633.

Zug R and Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews of the Cambridge Philosophical Society 90: 89–111.

Zug R and Hammerstein P (2018) Evolution of reproductive parasites with direct fitness benefits. Heredity 120: 266–281.

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.

Moran NA , McCutcheon JP and Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42: 165–190.

Perlman SJ , Hodson CN , Hamilton PT , Opit GP and Gowen BE (2015) Maternal transmission, sex ratio distortion, and mitochondria. Proceedings of the National Academy of Sciences of the United States of America 112: 10162–10168.

Vorburger C and Perlman SJ (2018) The role of defensive symbionts in host‐parasite coevolution. Biological Reviews of the Cambridge Philosophical Society 93: 1747–1764.

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. [doi: 10.1002/9780470015902.a0028327]