Integrated genomics and transcriptomics reveal molecular insights into extreme dietary adaptation in vampire bats

Abstract

Vampire bats are the only tetrapods that feed exclusively on blood. To uncover the molecular changes associated with this extreme dietary specialization, we generated six new reference genomes, including genomes of all three vampire bat species, and integrated comparative analyses of gene sequence evolution (selection signatures, duplications, and losses) with transcriptomic data from six major organs to identify shifts in gene expression. Our integrative analyses reveal sequence or expression changes in 150 genes that provide insights into the molecular biology of sanguivory. Through comparative analyses and experiments, we show that the enlarged vampire bat stomach has increased connective tissue content, likely facilitating extreme expansion, is pH-neutral, and exhibits reduced mucus production, together providing molecular insights into its shift from a digestive to an absorptive organ for water, electrolytes, and vitamins. We further uncover pathway-level molecular changes associated with altered gastrointestinal motility; trypsin-dependent protein digestion; upregulated amino acid catabolism with key aspects diverging from other mammals; impaired dietary fat digestion counterbalanced by increased fatty acid synthesis; defective sugar metabolism and natural insulin deficiency; enhanced heme iron absorption; and adult splenic erythropoiesis. Together, these findings provide an integrated view of molecular changes associated with one of the most extreme dietary transitions among vertebrates.