Natural selection on immune defense: A field experiment

Abstract

Predicting the evolution of phenotypic traits requires an understanding of natural selection on them. Despite its indispensability in the fight against parasites, selection on host immune defense has remained understudied. Theory predicts immune traits to be under stabilizing selection due to associated trade-offs with other fitness-related traits. Empirical studies, however, report mainly positive directional selection. This discrepancy could be caused by low phenotypic variation in the examined individuals and/or variation in host resource level that confounds trade-offs in empirical studies. In a field experiment where we maintained Lymnaea stagnalis snails individually in cages in a lake, we investigated phenotypic selection on two immune defense traits, phenoloxidase (PO)-like activity and antibacterial activity, in hemolymph. We used a diverse laboratory population and manipulated snail resource level by limiting their food supply. For six weeks, we followed immune activity, growth, and two fitness components, survival and fecundity of snails. We found that PO-like activity and growth were under stabilizing selection, while antibacterial activity was under positive directional selection. Selection on immune traits was mainly driven by variation in survival. The form of selection on immune defense apparently depends on the particular trait, possibly due to its importance for countering the present parasite community.

Potential for adaptation to climate change: family-level variation in fitness-related traits and their responses to heat waves in a snail population

“…Such studies can also be confounded by the direct effects of temperature on parasite transmission stages [65–68]. The examined immune parameters are central in the immune system of invertebrates, including molluscs [69–72] and are known to respond to various immune elicitors [73] as well as to be subject to natural selection [74] in L. stagnalis .…”

Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection

“…The examined immune parameters are central in the immune system of invertebrates, including mollusks (e.g. Butt & Raftos, ; Hellio, Bado‐Nilles, Gagnaire, Renault, & Thomas‐Guyon, ; Le Clec'h, Anderson, & Chevalier, ; Mitta, Vandenbulcke, & Roch, ), and are known to respond to various immune elicitors (Seppälä & Leicht, ) as well as to be subject to natural selection in L. stagnalis (Langeloh et al., ). It is, however, important to note that the role of these traits in determining resistance against E. aconiatum is not known.…”

“…We used structural equation modeling in IBM SPSS AMOS 23 (IBM, Armonk, NY, USA) to examine the effects of snail size, food consumption, respiration rate, and the examined immune parameters (PO‐like activity and antibacterial activity of hemolymph) as well as the causality of those effects on the snails' attractiveness to parasite cercariae and their susceptibility to infection. The original model was based on our estimates of the causality of possible impacts and included the following links between the variables: effects of snail size on food consumption (Salo, Stamm, Burdon, Räsänen, & Seppälä, ), respiration rate (Salo et al., ), attractiveness to parasites, immune function (both parameters (Salo et al., ; Seppälä & Jokela, )), and susceptibility to infection (Seppälä et al., ); effects of food consumption on attractiveness to parasites (Seppälä & Leicht, ), immune activity (both parameters (Langeloh et al., ; Seppälä & Jokela, )), and susceptibility to infection (Seppälä et al., ); effects of respiration rate on attractiveness to parasites and susceptibility to infection; effects of attractiveness to parasites and the level of immune parameters on susceptibility to infection. Additionally, the model included covariation between food consumption and respiration rate as well as between immune traits (Seppälä & Leicht, ).…”

“…As natural L. stagnalis populations often show low genetic diversity (Kopp, Wolff, & Jokela, 2012), we used snails from a genetically diverse laboratory population in this study. To create this population, we first established seven laboratory stock populations from adult snails collected from seven different ponds in northern Switzerland (see Langeloh, Behrmann-Godel, & Seppälä, 2017). We then combined 104 adult individuals of the F 2 laboratory generation from each stock population to form one mixed population.…”

“…Phenoloxidase (PO) enzymes are involved in the oxidative defense against mostly eukaryotic parasites (Cerenius & Söderhäll, 2004). Antibacterial activity, on the other hand, reflects the humoral immune response through antimicrobial proteins (Imler & Bulet, 2005 (Seppälä & Leicht, 2013) as well as to be subject to natural selection in L. stagnalis (Langeloh et al, 2017). It is, however, important to note that the role of these traits in determining resistance against E. aconiatum is not known.…”