Independent effects on cellular and humoral immune responses underlie genotype-by-genotype interactions between Drosophila and parasitoids

PLoS Pathog. 2019 Oct 7;15(10):e1008084. doi: 10.1371/journal.ppat.1008084. eCollection 2019 Oct.

Abstract

It is common to find abundant genetic variation in host resistance and parasite infectivity within populations, with the outcome of infection frequently depending on genotype-specific interactions. Underlying these effects are complex immune defenses that are under the control of both host and parasite genes. We have found extensive variation in Drosophila melanogaster's immune response against the parasitoid wasp Leptopilina boulardi. Some aspects of the immune response, such as phenoloxidase activity, are predominantly affected by the host genotype. Some, such as upregulation of the complement-like protein Tep1, are controlled by the parasite genotype. Others, like the differentiation of immune cells called lamellocytes, depend on the specific combination of host and parasite genotypes. These observations illustrate how the outcome of infection depends on independent genetic effects on different aspects of host immunity. As parasite-killing results from the concerted action of different components of the immune response, these observations provide a physiological mechanism to generate phenomena like epistasis and genotype-interactions that underlie models of coevolution.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / immunology*
  • Drosophila melanogaster / parasitology*
  • Female
  • Genotype
  • Hemocytes / immunology*
  • Hemocytes / parasitology
  • Host-Parasite Interactions*
  • Immunity, Humoral / immunology*
  • Male
  • Monophenol Monooxygenase / metabolism
  • Wasps / genetics
  • Wasps / immunology*
  • Wasps / pathogenicity

Substances

  • Monophenol Monooxygenase

Grants and funding

This work was funded by a Natural Environment Research Council grant NE/P00184X/1 to FMJ and ABL. ABL was supported by an EMBO Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.