Sociogenomics of maternal care and parent-offspring coadaptation in the European earwigs (Forficula auricularia)

Conflict and cooperation are ubiquitous in nature and in animal families where parents and offspring reciprocally influence each other's behavior and fitness. Evolutionary models predict selection for parent-offspring coadaptation that strike balance between parents pursuing self-fitness versus offspring demanding parental investment. Ultimately, it facilitates well-coordinated parenting and optimized cooperation with their offspring in the face of sexual reproduction and genetic recombination which cause genetic conflict. However, the genomic basis of parent-offspring coadaptation is poorly understood. My dissertation focused on the sociogenomics of materanl care and parent-offspring coadaptation in the European earwig (Forficula auricularia), a facultative uni-parental female care insect.
In the first chapter, we sequenced the transcriptome of the European earwig from various tissues and developmental stages of female and male applying Roche 454 pyrosequencing and Illumina HiSeq. The reads were de novo assembled independently and screened for possible microbial contamination and repeated elements. Hybrid assembly of these data yield comprehensive transcriptome with a low level of fragmentation comparing to the eukaryotic core gene dataset. More than 8,800 contigs of the hybrid assembly show significant similarity to insect-specific proteins and those were assigned for Gene Ontology terms. Finally, I validated the transcriptome and established a quantitative PCR method and applied it to homologs of five known sex-biased genes of the honeybee. The qPCR pilot study confirmed sex specific expression and also revealed significant expression differences between the brain and antenna tissue samples. The transcriptome presented here offers new opportunities to study the molecular bases and evolution of parental care and sociality in arthropods.
In the second chapter, I identified two parent-offspring coadapted genes, PebIII and Th, in the European earwig, based on comparative transcriptomics from experimentally manipulated mother-offspring interactions. Functional study applying RNAi revealed that PebIII in offspring enhances survival, in mothers enhances their relative investment in future reproduction and indirectly delayed offspring development; Th in mothers enhanced food provisioning, in offspring indirectly enhanced the likelihood of maternal future reproduction. These results suggested PebIII being reciprocally selfish while Th being reciprocally altruistic in both mothers and offspring. Metabolic pathway analyses further indicated the role of Th-restricted dopaminergic reward, PebIII mediated chemical perception and regulations between insulin signaling, juvenile hormone and vitellogenin in parent-offspring coadaptation and social evolution.
In the third chapter, I manipulated the interaction between earwig mothers and offspring over two generation and investigated transgenerational effects of maternal care on the expression of the two parent-offspring coadapted genes found in chapter2 and the fitness consequences in mothers and offspring. Significant transgenerational effects were found for the expression of PebIII and Th in the head of mothers. The expression of PebIII in the whole body of offspring showed significant effects of transgeneration treatment, current generation treatment and current generation by transgeneration treatments interaction. Significant transgenerational effect was found for relative maternal investment in future reproduction and offspring growth rate. Maternal future reproduction and latency for maternal future reproduction showed significant effects of current generation parental care treatment. Our results indicates an epigenetic regulation of gene expressions underlying parent-offspring coadaptation.
In the last chapter, the expressions of parent-offspring coadapted genes were validated using Fluidigm gene expression dynamic array. An additional treatment was included to control for time effect. We found the regulation of Th and PebIII were not influenced by the interaction between parent and offpsirng per se, but rather controlled by the reproductive stage of mothers suggesting preprogrammed expression in earwig. Such regulation of parenting genes in the sub-social species might be ancestral to the age-dependent division of labor in eusocial system.
These four chapters of my thesis were a series of continuous work and provided significant insights into the genomic basis of parent-offspring coadaptation. I established qPCR method to validate the de novo hybrid assembled transcriptome of the European earwig. I identified candidate parent-offspring coadapted genes using comparative trascriptomics. I established the method of Fluidigm gene expression dynamic array for earwigs to validate the RNA-Seq results. I established the RNAi techonology for earwigs to manipulate gene expressions and to study the social function of candidate genes. I demonstrated that PebIII and Th are two parent-offspring coadapted genes, which are co-regulated in mothers and offspring during active post-hatching parental care. Their expression were preprogrammed in mothers, reflecting the reproductive stage of females. Both genes showed causal effects on the behavior and fitness of earwig mothers and nymphs, coordinating the selfishness and altruism in family life. I showed transgenerational effects of maternal care on the expression of PebIII and Th, and opened the door for future studies of the epigenetic mechanisms regulating gene expression over generations and maintaining parent-offspring coadaptation in earwigs.