Cross-continental experimental infections reveal distinct defence mechanisms in populations of the three-spined stickleback Gasterosteus aculeatus.

Agnes Piecyk,Megan A Hahn,Olivia Roth,Nolwenn M Dheilly,David C Heins,Martin Kalbe,Michael A Bell

doi:10.1098/rspb.2021.1758

Abstract

Epidemiological traits of host–parasite associations depend on the effects of the host, the parasite and their interaction. Parasites evolve mechanisms to infect and exploit their hosts, whereas hosts evolve mechanisms to prevent infection and limit detrimental effects. The reasons why and how these traits differ across populations still remain unclear. Using experimental cross-infection of three-spined stickleback Gasterosteus aculeatus and their species-specific cestode parasites Schistocephalus solidus from Alaskan and European populations, we disentangled host, parasite and interaction effects on epidemiological traits at different geographical scales. We hypothesized that host and parasite main effects would dominate both within and across continents, although interaction effects would show geographical variation of natural selection within and across continents. We found that mechanisms preventing infection (qualitative resistance) occurred only in a combination of hosts and parasites from different continents, while mechanisms limiting parasite burden (quantitative resistance) and reducing detrimental effects of infection (tolerance) were host-population specific. We conclude that evolution favours distinct defence mechanisms on different geographical scales and that it is important to distinguish concepts of qualitative resistance, quantitative resistance and tolerance in studies of macroparasite infections.

Highlights

Epidemiological traits characterize the interaction and distribution of hosts and parasites and are shaped through the effects of the host, the parasite, their interaction and their environment [1,2,3,4]
Resistance reduces the likelihood of infection or limits parasite replication or growth, whereas tolerance limits the negative effects of a given parasite burden without reducing parasite replication or growth [4,8,9,10,11]
We show that the distinction between qualitative resistance, quantitative resistance and tolerance is of central importance in macroparasite infections

Summary

Introduction

Epidemiological traits characterize the interaction and distribution of hosts and parasites and are shaped through the effects of the host, the parasite, their interaction and their environment [1,2,3,4]. Host and parasite genotypes and allele frequencies change over evolutionary timescales, the response of an individual to different environmental conditions (known as ‘reaction norm’) is plastic. Understanding evolutionary dynamics and variation in host and parasite genetic and plastic effects on infection outcomes is crucial in basic science and clinical settings [5,6]. Parasites rely on host resources and evolve mechanisms increasing their ability to infect and to exploit their hosts [7]. Natural selection favours parasite traits that increase their fitness through trade-offs involving infectivity, growth and transmission. Hosts evolve defence mechanisms to resist and to tolerate parasites. Parasite prevalence is expected to decrease if hosts evolve resistance, whereas parasite prevalence may increase if hosts evolve tolerance [14,15]. We propose that suppression of the parasite’s growth is a important hitherto understudied form of quantitative resistance

Results

Discussion

Conclusion