Maternal patterns of inheritance alter transcript expression in eggs

Abstract

ABSTRACTModifications to early development can lead to evolutionary diversification. The early stages of development are under maternal control, as mothers produce eggs loaded with nutrients, proteins and mRNAs that direct early embryogenesis. Maternally provided mRNAs are the only expressed genes in initial stages of development and are known to be tightly regulated. Differences in maternal mRNA provisioning could lead to phenotypic changes in embryogenesis and ultimately evolutionary changes in development. However, the extent to which variation in maternal mRNA provisioning impacts ontogeny or life-history is unknown. Here, we use a species with dimorphic development— where females make eggs and larvae of different sizes and life-history modes—to investigate the extent of variation in maternal mRNA provisioning to the egg. We examine the effect of gene expression differences on subsequent generations of egg provisioning and determine the regulatory architecture underlying mRNA provisioning differences. We find that there is significant variation in gene expression across eggs of different development modes, and that both parent-of-origin and allele-specific effects contribute to mRNA expression differences. We also find that offspring of intraspecific crosses differentially provision their eggs based on their parents’ cross direction. This effect of allelic expression based on parent-of-origin has not been previously demonstrated in reproductive traits like oogenesis.AUTHOR SUMMARYVariation in early developmental programs can provide the basis for evolutionary diversification. In the early embryo, cellular functions are carried out by proteins and transcripts contributed by the mother to the egg until the embryo’s own genome can take over. Since these maternal factors are responsible for setting up all of the subsequent development of the offspring, they tend to be tightly regulated. However, variation exists in the amount and types of transcripts mothers provide. Here we examine how the variation in maternal transcripts that occurs in eggs of the speciesStreblospio benedicti, leads to developmental differences.S. benedictioffspring follow one of two distinct developmental programs that originate with egg size differences. We find significant variation in maternally provided transcripts correlated with the two life-histories, and that some of this variation in egg transcripts is directly related to the developmental type of the mother’s own parents. This parental effect on how mothers provide transcripts to their eggs has not previously been described and indicates the possibility for an offspring’s grandparents to affect their early developmental program by modulating the transcripts their mother provides.