Parasite‐mediated selection in a natural metapopulation of Daphnia magna

Abstract

Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, nonadaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a QST–FST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.

Demographic history shapes genomic variation in an intracellular parasite with a wide geographic distribution

“…Although several of these factors likely contributed to the Ne dynamics of H. tvaerminnensis, it is unclear which of them predominated. For example, D. magna varies strongly in susceptibility to H. tvaerminnensis, with the most susceptible hosts occurring in unstable habitats that have a high propensity to dry up in summer (like ephemeral rock or desert pools) (Cabalzar et al, 2019;Lange et al, 2015). These unstable habitats are also associated with frequent population extinctions and recolonizations as well as a loss of diversity because of frequent population bottlenecks.…”

Genetic slippage after sex maintains diversity for parasite resistance in a natural host population

“…Due to dominance and epistasis in the genetic architecture of resistance, this reshuffling resets the clock to the time before selection acted, rendering the response to selection zero. Although this is an extreme case of genetic slippage in response to sex, it is a powerful agent to maintain genetic diversity, which is a hallmark of resistance in natural populations of Daphnia and other animals, plants and bacteria (Altermatt and Ebert 2008;Desai and Currie 2015;Zhao et al 2016;Cabalzar et al 2019;Broniewski et al 2020;Sallinen et al 2020;White et al 2020). As climatic seasonality seems to determine the dynamics of parasite resistance in our host population, and given the known impact of climate change on epidemics in the D. magna-P. ramosa system (Auld and Brand 2017), one may speculate that the dynamics in our study population may change in response to the predicted changes in climatic conditions and seasonality.…”

“…Together with the consistency of our observed pattern, these facts suggest that genetic drift plays only a very minor role in shaping the yearly resistotype dynamics in the Aegelsee D. magna population and that the observed changes are the result of adaptive evolution, which is not always the case in the Daphnia system. In a rock pool metapopulation of D. magna, for example, with populations of small effective and census sizes, gene flow and strong founder effects create more sensitivity to drift, with a relatively weak signal of adaptive evolution (Cabalzar et al 2019).…”

A two-locus system with strong epistasis underlies rapid parasite-mediated evolution of host resistance

“…We added µL of 10-% Chelex solution and µL of proteinase K and incubated samples for two hours at 55 °C followed by 10 min at 99 °C. Fragment amplification, genotyping and allele scoring was done following the protocol described in Cabalzar et al (2019) (see Supplementary Markers Table S22 for PCR reaction details).…”