Parent and offspring genotypes influence gene expression in early life

Parents can have profound effects on offspring fitness. Little, however, is known about the mechanisms through which parental care variation influences offspring physiology in natural systems. White-throated sparrows Zonotrichia albicollis (WTSPs) exist in two genetic morphs, tan and white, controlled by a large polymorphic supergene. Morphs mate disassortatively, resulting in two pair types: tan male x white female (TxW) pairs, which provide biparental care and white male x tan female (WxT) pairs, which provide female-biased care. To investigate the effects of parental care variation, we performed RNA-seq on WTSP nestlings sampled from nests of both pair types. Pair type had the largest effect on nestling gene expression, with 881 genes differentially expressed (DE) and seven correlated gene co-expression modules. The DE genes and modules up-regulated in nests with female-biased parental care primarily function in metabolism and stress-related pathways resulting from the overrepresentation of stress response and proteolysis genes. These results show that parental genotypes, a proxy for parental care in this system, alter nestling physiology and highlight avenues of further research investigating the ultimate implications of alternative parental care strategies. Nestlings also exhibited morph-specific gene expression, driven by innate immunity genes and co-expression of genes located in the supergene. Remarkably, we identified the same regulatory hub genes in these blood-derived expression networks as were previously identified in WTSP brains (EPM2A, BPNT1, TAF5L). These hub genes were located within the supergene, highlighting the importance of this gene complex in structuring regulatory networks across diverse tissues.