Estimating Genetic and Maternal Effects Determining Variation in Immune Function of a Mixed-Mating Snail

Seppälä, Otto; Langeloh, Laura

doi:10.1371/journal.pone.0161584

Cited by 11 publications

(15 citation statements)

References 64 publications

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“…It is important to note that in studies utilising maternal sibships, such variation could arise not only due to additive genetic variance but also due to dominance variance and/or non-genetic maternal effects (see [35]). In our study system, however, the latter effects have been reported to be very weak in determining the variation in the examined traits [36]. In studies conducted using other organisms, the effect of challenging environmental conditions on the amount of genetic variation in key life history traits in natural populations has been shown to vary [14].…”

Section: Discussionmentioning

confidence: 95%

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

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Seppälä

2017

BMC Evol Biol

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BackgroundOn-going global climate change poses a serious threat for natural populations unless they are able to evolutionarily adapt to changing environmental conditions (e.g. increasing average temperatures, occurrence of extreme weather events). A prerequisite for evolutionary change is within-population heritable genetic variation in traits subject to selection. In relation to climate change, mainly phenological traits as well as heat and desiccation resistance have been examined for such variation. Therefore, it is important to investigate adaptive potential under climate change conditions across a broader range of traits. This is especially true for life-history traits and defences against natural enemies (e.g. parasites) since they influence organisms’ fitness both directly and through species interactions. We examined the adaptive potential of fitness-related traits and their responses to heat waves in a population of a freshwater snail, Lymnaea stagnalis. We estimated family-level variation and covariation in life history (size, reproduction) and constitutive immune defence traits [haemocyte concentration, phenoloxidase (PO)-like activity, antibacterial activity of haemolymph] in snails experimentally exposed to typical (15 °C) and heat wave (25 °C) temperatures. We also assessed variation in the reaction norms of these traits between the treatments.ResultsWe found that at the heat wave temperature, snails were larger and reproduced more, while their immune defence was reduced. Snails showed high family-level variation in all examined traits within both temperature treatments. The only negative genetic correlation (between reproduction and antibacterial activity) appeared at the high temperature. However, we found no family-level variation in the responses of most examined traits to the experimental heat wave (i.e. largely parallel reaction norms between the treatments). Only the reduction of PO-like activity when exposed to the high temperature showed family-level variation, suggesting that the cost of heat waves may be lower for some families and could evolve under selection.ConclusionOur results suggest that there is genetic potential for adaptation within both thermal environments and that trait evolution may not be strongly affected by trade-offs between them. However, rare differences in thermal reaction norms across families indicate limited evolutionary potential in the responses of snails to changing temperatures during extreme weather events.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0988-x) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 95%

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

Leicht

Seppälä

2017

BMC Evol Biol

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“…In our experiment, PO-like activity of snail hemolymph was under stabilizing selection, whereas antibacterial activity of hemolymph was under positive directional selection. Previous evidence for family-level genetic variation in the examined immune traits as well as in parasite resistance (Seppälä and Jokela 2010;Seppälä et al 2011;Seppälä and Langeloh 2016) suggests that snails should be able to respond to the selection described in this study. Our findings also suggest that different immune traits can differ with respect to their importance for hosts, which may depend on the types of parasites the hosts are exposed to as well as trade-offs associated with them.…”

Section: Pomentioning

confidence: 57%

“…It has previously been shown to display genetic variation both in immune function and in parasite resistance observed as variation among maternal sibships (Seppälä and Jokela ; Seppälä et al. ) as well as full‐sib families (Seppälä and Langeloh ; L. Langeloh, unpubl. data).…”

Section: Methodsmentioning

confidence: 99%

“…Apart from being a common prey species for fish and water fowl (Boycott 1936), L. stagnalis is a natural host to a large number of parasite species, including several castrating trematodes (Erasmus 1972;Väyrynen et al 2000). It has previously been shown to display genetic variation both in immune function and in parasite resistance observed as variation among maternal sibships (Seppälä and Jokela 2010;Seppälä et al 2011) as well as full-sib families (Seppälä and Langeloh 2016;L. Langeloh, unpubl.…”

Section: Study Organism and Experimental Animalsmentioning

confidence: 99%

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Natural selection on immune defense: A field experiment

2017

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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.

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“…Such differential tolerance is usually attributed to heritable genetic variation, non-genetic maternal effects or developmental plasticity that contribute to phenotypic variation. Given that sexual and asexual M. tuberculata can coexist in natural populations [ 26 ], disentangling between genetic and non-genetic variation requires genotyping the snails to determine whether they were produced through outcrossing or parthenogenetically [ 45 ]. However, in this study three of the six populations are known to harbor very few distinct clones, i.e.…”

Section: Discussionmentioning

confidence: 99%

Cost of resistance to trematodes in freshwater snail populations with low clonal diversity

2017

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BackgroundThe persistence of high genetic variability in natural populations garners considerable interest among ecologists and evolutionary biologists. One proposed hypothesis for the maintenance of high levels of genetic diversity relies on frequency-dependent selection imposed by parasites on host populations (Red Queen hypothesis). A complementary hypothesis suggests that a trade-off between fitness costs associated with tolerance to stress factors and fitness costs associated with resistance to parasites is responsible for the maintenance of host genetic diversity.ResultsThe present study investigated whether host resistance to parasites is traded off with tolerance to environmental stress factors (high/low temperatures, high salinity), by comparing populations of the freshwater snail Melanoides tuberculata with low vs. high clonal diversity. Since polyclonal populations were found to be more parasitized than populations with low clonal diversity, we expected them to be tolerant to environmental stress factors. We found that clonal diversity explained most of the variation in snail survival under high temperature, thereby suggesting that tolerance to high temperatures of clonally diverse populations is higher than that of populations with low clonal diversity.ConclusionsOur results suggest that resistance to parasites may come at a cost of reduced tolerance to certain environmental stress factors.

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Estimating Genetic and Maternal Effects Determining Variation in Immune Function of a Mixed-Mating Snail

Cited by 11 publications

References 64 publications

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

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

Natural selection on immune defense: A field experiment

Cost of resistance to trematodes in freshwater snail populations with low clonal diversity

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