Roles of maternal effects in maintaining genetic variation: Maternal storage effect

Abstract

Understanding the maintenance of genetic variation remains a central challenge in evolutionary biology. Recent empirical studies suggest the importance of temporally varying selection, as allele frequencies have been found to fluctuate substantially in the wild. However, previous theory suggests that the conditions for the maintenance of genetic variation under temporally fluctuating selection are quite restrictive. Using mathematical models, we demonstrate that maternal genetic effects, whereby maternal genotypes affect offspring phenotypes, can facilitate the maintenance of polymorphism in temporally varying environments. Maternal effects result in mismatches between genotypes and phenotypes, thereby buffering the influence of selection on allele frequency. This decreases the magnitude of allele-frequency fluctuations and creates conditions for the maintenance of variation when selection causes fluctuations. Therefore, maternal effects may result in a temporal storage effect ("maternal storage effect"). On the other hand, when selection does not cause fluctuations (e.g., linear negative frequency-dependent selection), maternal genetic effects moderate the relative importance of selection compared to genetic drift and promote stochastic allele extinction in finite populations. Thus, maternal effects can play an important role in the maintenance of polymorphism, but the direction of the effect depends on the nature of selection.

Partial protection from cyclical selection generates a high level of polymorphism at multiple non‐neutral sites

“…Other mechanisms include sex‐limited traits (Reinhold ; Gorelick and Bertram ), the presence of a neighboring population with reduced magnitude of selection (Gulisija and Kim ), a modifier of phenotypic plasticity (Gulisija et al. ), and maternal effects (Yamamichi and Hoso ). This growing list of mechanisms suggests that the biological conditions for a storage effect—the existence of any pathway in the inheritance of a nonneutral allele that protects it from selection—may be more general than restricted.…”

“…One of the first studied was overlapping generations with age-or stagespecific selection, which can be extended to seed banks in plants or diapause in animals (Ellner and Hairston Jr 1994;Hedrick 1995;Ellner and Sasaki 1996;Turelli et al 2001;Svardal et al 2011). Other mechanisms include sex-limited traits (Reinhold 2000;Gorelick and Bertram 2003), the presence of a neighboring population with reduced magnitude of selection (Gulisija and Kim 2015), a modifier of phenotypic plasticity (Gulisija et al 2016), and maternal effects (Yamamichi and Hoso 2017). This growing list of mechanisms suggests that the biological conditions for a storage effect-the existence of any pathway in the inheritance of a nonneutral allele that protects it from selection-may be more general than restricted.…”

Towards a heuristic understanding of the storage effect

“…First, we contend that transgenerational plasticity (e.g., maternal effects, epigenetics) can carry the effects of the environment forward through time, therefore satisfying ingredient 3B. Note that what we are proposing here is different from the the model of Yamamichi and Hoso, 2017, where maternal effects (a type of transgenerational plasticity) produces a negative interaction effect and diploidy leads to the EC covariance. Even though transgenerational plasticity can generate an EC covariance, plasticity of any type is not likely to evolve in a quickly changing environment (Stomp et al, 2008).…”

“…However, an interaction effect can arise in models without population structure or overlapping generations, purely due to a multiplicative form of the per capita growth rate function (Li and Chesson, 2016;Letten et al, 2018;Ellner et al, 2019). It is also worth noting that the storage effect was originally discovered by population geneticists, and that in the population genetic version of the storage effect, an interaction effect can result from heterozygosity (Dempster, 1955;Haldane and Jayakar, 1963), sex-linked alleles (Reinhold, 2000), epistasis (Gulisija et al, 2016), and maternal effects (Yamamichi and Hoso, 2017). In summary, there are many ways for an interaction effect to occur.…”

The storage effect is not about bet-hedging or population stage-structure

“…Chesson and Huntly (1988) write, "... iteroparous plant and sessile marine organisms, can buffer by participating in reproduction over a number of years... Semelparous species can experience these buffering effects if the offspring of an individual mature over a range of years..." More generally, a negative interaction effect may arise from other forms of population structure: dormancy (Cáceres, 1997;Ellner, 1987), phenotypic variation (Chesson, 2000b), or spatial variation (Chesson, 2000a). In studies of the population genetic storage effect (which promotes allelic diversity), negative interaction effects can be produced by heterozygotes (Dempster, 1955;Haldane and Jayakar, 1963), sex-linked alleles (Reinhold, 2000), epistasis (Gulisija et al, 2016), and maternal effects (Yamamichi and Hoso, 2017).…”