Abstract
Adaptation to specialized diets often requires modifications at both genomic and microbiome levels. We applied a hologenomic approach to the common vampire bat (Desmodus rotundus), one of the only three obligate blood-feeding (sanguivorous) mammals, to study the evolution of its complex dietary adaptation. Specifically, we assembled its high-quality reference genome (scaffold N50 = 26.9 Mb, contig N50 = 36.6 kb) and gut metagenome, and compared them against those of insectivorous, frugivorous and carnivorous bats. Our analyses showed a particular common vampire bat genomic landscape regarding integrated viral elements, a dietary and phylogenetic influence on gut microbiome taxonomic and functional profiles, and that both genetic elements harbour key traits related to the nutritional (for example, vitamin and lipid shortage) and non-nutritional (for example, nitrogen waste and osmotic homeostasis) challenges of sanguivory. These findings highlight the value of a holistic study of both the host and its microbiota when attempting to decipher adaptations underlying radical dietary lifestyles.
Highlights
IntroductionThe order Chiroptera (bats) exhibits a wide variety of dietary specializations, and includes the only three obligate bloodfeeding mammalian species, the vampire bats (family Phyllostomidae, subfamily Desmodontinae)
The order Chiroptera exhibits a wide variety of dietary specializations, and includes the only three obligate bloodfeeding mammalian species, the vampire bats
When compared to the other bats, we identified an enrichment in the common vampire bat microbial genes involved in response to low nutrient availability (RelA/SpoT family protein, Fisher’s P =0 .0064, and guanosine pentaphosphate, Fisher’s P =0 .0018), and enzymes in the common vampire bat core involved in the reverse Krebs cycle (Supplementary Information 10), which is used by some bacteria to produce carbon compounds from CO2 and water
Summary
The order Chiroptera (bats) exhibits a wide variety of dietary specializations, and includes the only three obligate bloodfeeding mammalian species, the vampire bats (family Phyllostomidae, subfamily Desmodontinae). Vampire bats have evolved numerous key physiological adaptations to this lifestyle, for which the associated genomic changes have not yet been fully characterized due to the lack of an available reference genome These adaptations include morphological specializations (such as claw-thumbed wings and craniofacial changes including sharp incisors and canines), infrared sensing capacity[3] for the identification of accessible blood vessels in prey[4], and renal adaptations to the high protein content in its diet[5] (such as a high glomerular filtration rate and effective urea excretion). In response to the growing awareness of the key roles that host–microbiome relationships can play across the spectra of life, various studies have advocated for the ‘hologenome’ concept[18,19,20] This argues that natural selection acts on both the host and its microbiome (together forming the holobiont); evolutionary studies should incorporate both. The extreme dietary adaptation of vampire bats provides a suitable model to investigate the effect of selection across the genome and microbiome, and allows exploration of the role of host-associated microbiome in the evolution of specialized diets
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