Ecological and genetic variation in immune activity of an invertebrate in the wild
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Date
2023
Publication Type
Doctoral Thesis
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Abstract
Parasites pose a severe threat to organisms by reducing their fitness. The immune system is the primary barrier against infections. However, immune activity varies among individuals in the wild. Both ecological and genetic factors can contribute to this variation. Relevant ecological factors include, for example, exposure to infections, resource availability and temperature. On the other hand, a specific part of genetic variance determining immune trait values, additive genetic variance, defines the evolutionary potential of immune function in a population. To predict how populations can respond to parasite-mediated selection, estimating the relative proportions of additive genetic and environmental variance in explaining immune activity in nature is needed. Unfortunately, most earlier research investigating the influence of environmental and genetic factors on immune activity has been conducted under laboratory conditions. The freshwater snail Lymnaea stagnalis provides a good model system to examine the relative roles of ecological and genetic factors in immune activity in the wild. First, snails show large individual-level variation in the levels of immune defense traits and life history traits. Second, both ecological and genetic factors are important drivers of variation in immune activity based on lab studies. Third, snail populations are continuously challenged by parasites such as trematodes. Fourth, methods for quantifying different components of snail immune activity have been developed in earlier work.
This thesis investigates ecological and genetic factors that may drive among-individual variation in snail immune defense traits in the wild. First, I examined the population genetic structure and drivers of genetic diversity (i.e., demographic effects, mating system) in five natural snail populations. Understanding such processes is important because they can limit populations’ genetic potential for evolution. Using RAD-seq data, I found strong genetic differentiation among populations and excess homozygosity despite the low selfing rates and relatedness estimates in all populations. The results suggest that extinction-recolonisation dynamics that lead to genetic drift may play a larger role than the mating system in defining the genetic diversity in L. stagnalis populations. This genetic drift may limit the evolutionary potential in individual populations. Second, I investigated ecological factors driving among-individual variation in the levels of oxidative and antibacterial components of the snail immune system in two of the above populations. I also asked if the expression of these components of defense are traded off. I sampled the populations six times throughout one reproductive season and measured snail immune activity, size (shell length), resource level (fat content), and trematode infection status (a proxy for infection risk at the population level). I tested if snails (uninfected individuals) differed in their immune activity (1) between populations and (2) over time, and if these effects arose from differences in (3) risk of exposure to trematode parasites, (3) variation in snail condition/resource level and/or (4) trade-offs between different immunological mechanisms. Antibacterial activity varied over time, and it was the highest in the mid-season. Temporal variation in oxidative defense (PO activity) did not show a clear pattern. I found between population differences in snail condition/resources but not in immune activity. Additionally, there was a trade-off between oxidative and antibacterial immune activity.
These results suggest that the among-individual differences in the expression of immune activity do not depend on the local environment but more on individual-level constraints. Third, I examined if the observed among-individual variation in immune activity had (1) an additive genetic basis and (2) if there were genetic trade-offs between the immune traits using one of the above populations. These genetic properties are critical in determining the evolutionary potential of immune function when subject to parasite-mediated selection. Previous research on the evolutionary potential of immune defense traits has utilised breeding designs conducted under lab conditions or social pedigrees available for a few natural vertebrate populations. Using high-marker density genotyping (ddRAD-seq), I estimated the additive genetic variance (i.e., evolutionary potential) in immune activity and the covariance between immune traits in a natural invertebrate population. I used 19,336 SNP markers to generate a genomic relatedness matrix for 561 snails. Then, I estimated the additive genetic variance and the covariance in snail immune traits using this matrix. I found evolutionary potential in snail immune activity, although their heritability estimates were low. Interestingly, estimates for the evolutionary potential of oxidative defense increased towards the late season. The examined immune traits did not show genetic trade-offs, suggesting their independent evolution. I found evolutionary potential in snail immune activity despite the strong effect of genetic drift on the studied population. However, the role of the environmental variation was larger than the additive genetic variation. I found that individual-level constraints related to resources rather than local environment (i.e., population and time of the season) likely shapes among-individual variation in immune activity. I did not detect a genetic basis for the trade-off between oxidative and antibacterial defense which was shown at the phenotypic level in both populations. Context-dependency of the evolutionary potential in oxidative defense was evident in variation in additive variance over time.
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Examiner: Jokela, Jukka
Examiner : Seppälä, Otto Eerikki
Examiner : Feulner, Philine G.D.
Examiner : Johnston, Susan E.
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ETH Zurich
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Subject
Quantitative genetics; Ecological genetics; POPULATION GENETICS (ZOOLOGY); IMMUNE DEFENCE (PARASITOLOGY, IMMUNOLOGY); natural populations; Field data; RAD sequencing
Organisational unit
03705 - Jokela, Jukka / Jokela, Jukka
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Funding
ETH-20 17-1 - Molecular quantitative genetics of invertebrate immune function (ETHZ)