Parallel and costly changes to cellular immunity underlie the evolution of parasitoid resistance in three Drosophila species

Abstract

A priority for biomedical research is to understand the causes of variation in susceptibility to infection. To investigate genetic variation in a model system, we used flies collected from single populations of three different species of Drosophila and artificially selected them for resistance to the parasitoid wasp Leptopilina boulardi, and found that survival rates increased 3 to 30 fold within 6 generations. Resistance in all three species involves a large increase in the number of the circulating hemocytes that kill parasitoids. However, the different species achieve this in different ways, with D. melanogaster moving sessile hemocytes into circulation while the other species simply produce more cells. Therefore, the convergent evolution of the immune phenotype has different developmental bases. These changes are costly, as resistant populations of all three species had greatly reduced larval survival. In all three species resistance is only costly when food is in short supply, and resistance was rapidly lost from D. melanogaster populations when food is restricted. Furthermore, evolving resistance to L. boulardi resulted in cross-resistance against other parasitoids. Therefore, whether a population evolves resistance will depend on ecological conditions including food availability and the presence of different parasite species.

Host-pathogen coevolution increases genetic variation in susceptibility to infection

“…In humans this has been proposed as an explanation of why there is less genetic variation in susceptibility to pathogens that are effectively controlled by the adaptive immune response, as these resistance mechanisms may be less costly (Baker and Antonovics, 2012). However, it seems unlikely that virus resistance in Drosophila is costly, as experiments have failed to detect costs of DCV resistance (Faria et al, 2015) despite costs of parasitoid and bacterial resistance being repeatedly detected (McGonigle et al, 2017; McKean et al, 2008; Ye et al, 2009). Sigma viruses are also extreme host specialists, so evolutionary changes in resistance will tend to alter pathogen prevalence and so the strength of selection.…”

Sexual selection reveals a cost of pathogen resistance undetected in life‐history assays

“…This notion underlies the theory of optimal immune defense (e.g., Viney et al 2005;Donnelly et al 2017), as well as some of the theories linking heritable pathogen resistance with sexually selected traits (Folstad and Karter 1992;Westneat and Birkhead 1998;Adamo and Spiteri 2005). It is supported by extensive evidence from genetic analyses and selection experiments that found negative genetic correlations between pathogen resistance and survival, growth, developmental rate, fecundity or longevity, often amplified under nutritional or other stress (Kraaijeveld and Godfray 2008;Vorburger et al 2008;Modak et al 2009;Ye et al 2009;Hall et al 2010;Boots 2011;Duncan et al 2011;Auld et al 2013;Vijendravarma et al 2015;McGonigle et al 2017;McNamara and Simmons 2017;Bartlett et al 2018; older studies reviewed in Lazzaro and Little 2009).…”

“…; McGonigle et al. ; McNamara and Simmons ; Bartlett et al. ; older studies reviewed in Lazzaro and Little ).…”

Variation in intrinsic resistance of pea aphids to parasitoid wasps: A transcriptomic basis

“…The majority of work in this area comes from Drosophila species, in which capacity to evolve increased immunity against different common parasitoid threats has been demonstrated by experimental evolution [12]. In these studies, evolution of greater parasitoid resistance is correlated with increasing hemocyte numbers [9,13]. Identifying molecular mechanisms involved in resistance across a broader variety of host-enemy interactions and studying how these mechanisms vary within host species is critical for understanding how insect immune systems evolve.…”