Nuclear-mitochondrial interactions and gene expression in hybrid honey bees (Apis mellifera)

Invasive Africanized honey bees are hybrids between African and European subspecies (primarily Apis mellifera scutellata and A.m. ligustica). Hybrids produced from genetically isolated lineages form two reciprocal families, equivalent in their nuclear genomic makeup but differing in their mitochondrial origin, based on the mother’s lineage.  The mitochondrial genome evolves much faster than the nuclear genome, and this rate of evolution is particularly high in many hymenoptera (over 30 times higher than nuclear genes).  Despite this fast evolution, the mitochondrial-encoded genes (37 in most animals) must interact with many nuclear-encoded genes (upwards of 1200) during the biogenesis and maintenance of functioning mitochondria.  This difference in evolutionary rates of these genomes, as well as differences in response to selective pressure, can result in nuclear-mitochondrial incompatibilities in hybrids when the interacting genes have not evolved in the same lineage.

We sequenced the transcriptomes of honey bees from a cross between Africanized honey bees (themselves feral hybrids) and European honey bees (Apis mellifera carnica) and assessed both overall gene expression differences between the reciprocal families as well as allele-specific expression differences.  We found that there is an overrepresentation of mitochondrial-localizing genes that are biased toward expression of the allele that matches their mitochondrial type (i.e. European alleles are expressed more highly in bees with European mitochondria).  We explore the evolutionary scenarios that lead to this expression difference and postulate potential mechanisms for the expression differences.