Hologenomic adaptations underlying the evolution of sanguivorous (bloodthirsty) behavior in the common vampire bat

BATS are mammals that belong to the order Chiroptera (from the Latin prefix “chiro” meaning “hand”, and from the Greek word “ptera” which means “wings”) –– which refers to the pronounced elongation of finger digits that support the flying membrane). Bats are the only mammals to have achieved powered flight. Their arms are spindly, with membranes stretched between the finger bones on each hand. This arrangement makes their wings quite different from those of birds and ancient pterosaurs. In fact, bats have evolved flight quite independently. They also differ from other flying animals in their reliance on hearing for navigation; many bats use sonar echos to find their way around in caves and at night. Despite their resemblance to rodents (the German word for “bat” is “pfledermaus”, i.e. “flying mouse”), bats are not closely related to mice at all. Recent evidence suggests that they may be most closely related to primates. Bats are among the most successful groups of mammals: worldwide, there are nearly 1,000 species of bats –– making up about one quarter of all mammalian species.

Bats exhibit a wide variety of dietary specializations –– including insects, meat, fruits, and BLOOD. There are only three VAMPIRE (obligate blood-feeding) forms. Blood is a challenging dietary source because it consists of an ~78% liquid phase and a dry-matter phase comprising ~93% proteins, and only ~1% carbohydrates, providing extremely low levels of vitamins; a diet of blood also potentially contains blood-borne pathogens. Vampire bats have evolved numerous key physiological adaptations to this lifestyle, for which associated genomic changes have not yet been fully characterized (due to lack of an available reference genome). These adaptations include morphological specializations (such as claw-thumbed wings and craniofacial changes including sharp incisors and canine teeth), infra-red sensing capacity for identifying easily accessible blood vessels in their prey, and renal adaptations to the high protein content in its diet (such as a high glomerular filtration rate and effective urea excretion). Furthermore, given the high risk of exposure to blood-borne pathogens, another important trait in the vampire bat is its immune system.

Authors [see attached report] applied a holo-genomic approach to the common vampire bat (Desmodus rotundus), one of the only three obligate sanguivorous mammals, to study evolution of its complex dietary adaptation. Authors established the vampire bat’s high-quality reference genome, as well as its gut microbiome, and compared them against those of insect-eating, fruit-eating, and meat-eating bats. Their analyses showed a genomic landscape that included integrated viral elements, and a dietary and phylogenetic influence on gut microbiome taxonomic and functional profiles. Furthermore, both genetic elements harbor key traits related to the nutritional (e.g. vitamin and lipid shortage) and non-nutritional (e.g. nitrogen waste and osmotic homeostasis) challenges of sanguivory (lifestyle of blood-sucking). 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 –– although these little bloodsuckers would not consider their lifstyle as “radical”.

Nat Ecol Evol 2o18 Feb 19; doi: 10.1038/s415590018-0476-8

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