Sympatric and Allopatric Divergence of MHC Genes in Threespine Stickleback

Parasites can strongly affect the evolution of their hosts, but their effects on host diversification are less clear. In theory, contrasting parasite communities in different foraging habitats could generate divergent selection on hosts and promote ecological speciation. Immune systems are costly to maintain, adaptable, and an important component of individual fitness. As a result, immune system genes, such as those of the Major Histocompatability Complex (MHC), can change rapidly in response to parasite-mediated selection. In threespine stickleback (Gasterosteus aculeatus), as well as in other vertebrates, MHC genes have been linked with female mating preference, suggesting that divergent selection acting on MHC genes might influence speciation. Here, we examined genetic variation at MHC Class II loci of sticklebacks from two lakes with a limnetic and benthic species pair, and two lakes with a single species. In both lakes with species pairs, limnetics and benthics differed in their composition of MHC alleles, and limnetics had fewer MHC alleles per individual than benthics. Similar to the limnetics, the allopatric population with a pelagic phenotype had few MHC alleles per individual, suggesting a correlation between MHC genotype and foraging habitat. Using a simulation model we show that the diversity and composition of MHC alleles in a sympatric species pair depends on the amount of assortative mating and on the strength of parasite-mediated selection in adjacent foraging habitats. Our results indicate parallel divergence in the number of MHC alleles between sympatric stickleback species, possibly resulting from the contrasting parasite communities in littoral and pelagic habitats of lakes

Precise tuning of barnacle leg length to coastal wave action.

Both spatial and temporal variation in environmental conditions can favour intraspecific plasticity in animal form. But how precise is such environmental modulation? Individual Balanus glandula Darwin, a common northeastern Pacific barnacle, produce longer feeding legs in still water than in moving water. We report here that, on the west coast of Vancouver Island, Canada, the magnitude and the precision of this phenotypic variation is impressive. First, the feeding legs of barnacles from protected bays were nearly twice as long (for the same body mass) as those from open ocean shores. Second, leg length varied surprisingly precisely with wave exposure: the average maximum velocities of breaking waves recorded in situ explained 95.6-99.5% of the variation in average leg length observed over a threefold range of wave exposure. The decline in leg length with increasing wave action was less than predicted due to simple scaling, perhaps due to changes in leg shape or material properties. Nonetheless, the precision of this relationship reveals a remarkably close coupling between growth environment and adult form, and suggests that between-population differences in barnacle leg length may be used for estimating differences in average wave exposure easily and accurately in studies of coastal ecology

Appendix A. Location, size, and depth of stickleback lakes.

Location, size, and depth of stickleback lakes

Frequency distributions of MHC-class IIB alleles in each population.

<p>Panel (A) is the distribution for all the alleles identified in the study. Panel (B) is the distribution for the pelagic phenotype in Kennedy Lake. Panel (C) is the distribution for the intermediate phenotype in Cranby Lake. Panels (D) and (E) are the distributions for each stickleback species in the two lakes with species pairs.</p

Simulation output with varying selection strengths.

<p>Bar heights are the mean allele counts averaged over 10 simulations, and error bars denote one standard deviation. Simulations were run for 1000 generations with 10,000 individuals in each population. All alleles were initially present at equal frequencies. in all plots and recombination occurred freely between all loci. Selection strengths were, in the top plot: and , in the middle plot: and , and in the bottom plot: and .</p

Conclusions from the log-linear analysis in Table 2.

<p>Conclusions from the log-linear analysis in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010948#pone-0010948-t002" target="_blank">Table 2</a>.</p

Two scenarios leading to divergent selection on MHC genotype.

<p>Panel (A) shows the contrasting virulence distribution of two parasite communities, where the dotted line indicates that the average virulence of the community is similar in both environments. Panel (B) shows the tradeoff between the ability of the immune system to detect parasites (dotted lines) and the risk of T-cell depletion (solid lines). Panel (C) shows the tradeoff between allocating resources to the adaptive versus the innate immune system. Panel (D) illustrates the resulting population distribution of individual allele number in the two environments (A or B) resulting from divergent selection mediated by either of the tradeoffs illustrated in Panel B and C.</p

Allelic richness of MHC and microsatellites.

<p>Summary of the mean (MHC) and median (MHC) number of MHC class IIB alleles per individual, and the number of different alleles found in the sampled population (MHC). The number of alleles detected per sampled stickleback (AR) is a standardized index of population-level allelic richness, and was calculated via bootstrapping with a constant sampling effort (N = 20). Limnetics and benthics did not differ in the levels of heterozygosity (H and H), or in the mean number of alleles per microsatellite locus, calculated at both the population level (Rs) and at the individual level (Sats).</p

Frequency distributions of the number of MHC-class IIB alleles per individual.

<p>The top panels show the distribution of littoral and intermediate eco-types, and the bottom panels show the distribution of pelagic eco-types. Red points and bars indicate the mean population allelic richness ( SD).</p