Evolutionary genetics of maternal effects

Abstract

Maternal genetic effects (MGEs), where genes expressed by mothers affect the phenotype of their offspring, are important sources of phenotypic diversity in a myriad of organisms. We use a single-locus model to examine how MGEs contribute patterns of heritable and nonheritable variation and influence evolutionary dynamics in randomly mating and inbreeding populations. We elucidate the influence of MGEs by examining the offspring genotype-phenotype relationship, which determines how MGEs affect evolutionary dynamics in response to selection on offspring phenotypes. This approach reveals important results that are not apparent from classic quantitative genetic treatments of MGEs. We show that additive and dominance MGEs make different contributions to evolutionary dynamics and patterns of variation, which are differentially affected by inbreeding. Dominance MGEs make the offspring genotype-phenotype relationship frequency dependent, resulting in the appearance of negative frequency-dependent selection, while additive MGEs contribute a component of parent-of-origin dependent variation. Inbreeding amplifies the contribution of MGEs to the additive genetic variance and, therefore enhances their evolutionary response. Considering evolutionary dynamics of allele frequency change on an adaptive landscape, we show that this landscape differs from the mean fitness surface, and therefore, under some condition, fitness peaks can exist but not be "available" to the evolving population.

Keywords: Kin selection; Social effects; adaptive landscape; dominance; frequency dependent selection.

Figure 1

Evolution of overdominance with direct and maternal effects. These figures illustrate a case where there is a direct and a maternal effect of the same size showing only dominance (values are arbitrary, so the y axis is shown as unit free). (A) The red (dashed) line shows the “surface” of mean fitness, while the blue line (solid) shows the “realized adaptive landscape” that determines how the population evolves. (B) The change in allele frequency for a locus showing a direct or maternal dominance effect across allele frequency space. With either type of effect the population evolves to an internal equilibrium at p ₁ = 0.5 when there is allelic variation, but the direct effect (red, dashed) evolves to the equilibrium faster than the maternal effect (blue, solid), when started at the same gene frequency.

Figure 2

The offspring genotype–phenotype relationship for a maternal effect showing only dominance. (A) The expected offspring phenotype (fitness) for the three unordered offspring genotypes as a function of the frequency of the A ₁ allele. The heterozygote line represents the mean of the two reciprocal heterozygotes. It is always the case with maternal effect dominance that the mean fitness of the offspring heterozygote is midway between the two homozygotes. The fitness values are on an arbitrary scale and are not labeled (but are all positive). (B) The realized additive effect of the locus is shown as a function of the frequency of the A ₁ allele.

Figure 3

Evolution of a locus showing an additive direct effect and a dominance maternal effect that produce a peaked fitness surface. (A) The red (dashed) line shows the “surface” of mean fitness, where there is a peak at an allele frequency of 0.75. The blue (solid) line shows the “realized adaptive landscape” for maternal effects, which determines how the population evolves. Note that the realized adaptive landscape does not have a peak. (B) The change in allele frequencies at the A locus (Δp ₁) as a function of the frequency of the A ₁ allele, demonstrating that the population evolves to fixation of the A ₁ allele.