Isolation over 35 years in a heated biotest basin causes selection on MHC class IIß genes in the European perch (Perca fluviatilis L.)

Abstract

Genes that play key roles in host immunity such as the major histocompatibility complex (MHC) in vertebrates are expected to be major targets of selection. It is well known that environmental conditions can have an effect on host-parasite interactions and may thus influence the selection on MHC. We analyzed MHC class IIß variability over 35 years in a population of perch (Perca fluviatilis) from the Baltic Sea that was split into two populations separated from each other. One population was subjected to heating from cooling water of a nuclear power plant and was isolated from the surrounding environment in an artificial lake, while the other population was not subjected to any change in water temperature (control). The isolated population experienced a change of the allelic composition and a decrease in allelic richness of MHC genes compared to the control population. The two most common MHC alleles showed cyclic patterns indicating ongoing parasite-host coevolution in both populations, but the alleles that showed a cyclic behavior differed between the two populations. No such patterns were observed at alleles from nine microsatellite loci, and no genetic differentiation was found between populations. We found no indications for a genetic bottleneck in the isolated population during the 35 years. Additionally, differences in parasitism of the current perch populations suggest that a change of the parasite communities has occurred over the isolation period, although the evidence in form of in-depth knowledge of the change of the parasite community over time is lacking. Our results are consistent with the hypothesis of a selective sweep imposed by a change in the parasite community.

Keywords: MHC II; Perca fluviatilis; microsatellites; selection; time series; warming.

Figure 1

The study organism, the European perch Perca fluviatilis, is one of the most common freshwater fish in Europe. Picture taken by Fredrik Sundström, Department Animal Ecology, Uppsala University.

Figure 2

Map over the study area with the Biotest Lake and the control area (Forsmark).

Figure 3

Summary of the different possible outcomes with regard to MHC variability over time in the two populations. (A) No change in either population, (B) change in the heated population, but not in the control population, (C) a scenario where the temporal change in both populations is the same, (D) a scenario where the temporal change in both populations is different.

Figure 4

Relative frequency of the maximum number of MHC loci summed over all individuals and years in the Biotest Lake and Forsmark.

Figure 5

Allelic richness measured as the maximum number of alleles possible for (A) BT MHC and (B) FM MHC and MHC gene diversity for (C) BT, and (D) FM. The open dots are the observed values, the closed dots are the expected number based on rarefaction, and the dotted line represents the experiment wise 95% confidence interval. The vertical lines represent the year when heating started (left line) and the year when the barriers were open (right line). The time between these lines represent the time when the Biotest Lake was both heated and closed from migration.

Figure 6

Pairwise F_ST comparisons over time. Given are the year-by-year comparisons between Biotest Lake and Forsmark perch populations based on (A) microsatellite data and (B) MHC data. The within population pairwise F_ST comparisons based on MHC data where every year is compared to the first year (1977) for Biotest (C) and Forsmark (D). The dotted line is the experiment wise 95% interval. The vertical lines represent the year when heating started (left line) and the year when the barriers were open (right line).

Figure 7

Change of allele frequencies in the two most common MHC alleles in both populations over time. The time series in (A) and (B) are smoothed with a Parzen smoothing window size 5, and the graphs (C–D) using a moving average (N − 3) procedure. (A) allele 282 in BT with the model (dotted line) of Decaestecker et al. (2013) fitted to the data (solid line), (B) allele 286 in FM fitted with the same model, (C) alleles 282 and 286 in FM, (D) alleles 282 and 286 in BT. The vertical lines in (A) and (B) represent the year when heating started (left line) and the year when the barriers were open (right line).

Figure 8

Effective population size (N_e) in the (A) BT and (B) FM populations. Filled circles are the yearly estimates, and the open circles the yearly lower 2.5 percentiles. The solid horizontal line is the harmonic mean overall years, and the dotted line the harmonic mean of the lower 2.5 percentile overall years. The vertical lines represent the year when heating started (left line) and the year when the barriers were open (right line).