Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat

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.

Figure 1. Comparative genomic analyses.

Species with a light blue circle were used for comparison of TEs. Species used for the identification of putative lost genes are represented with a golden silhouette and their corresponding number of putatively lost genes compared to the human genome. The number of gene families under expansion (green) and contraction (red) in Chiroptera using E. europaeus as outgroup are indicated. Estimated dates of nodes (in million years) are indicated in black. The gut microbiomes of bats with different diets derive from Rousettus aegyptiacus (blue, frugivorous), Macroderma gigas (green, carnivorous), Rhinolophus ferrumequinum (grey, insectivorous), and the common vampire bat (red, sanguivorous).

Figure 2. Dietary challenges overcome by the common vampire bat.

(A) Adaptational contributions to sanguivory accountable to genomic changes alone (blue labels) and (B) adaptational contributions to sanguivory within a hologenomic context (blue labels for host genes, red labels for gut microbial traits).

Figure 3. Comparison of the taxonomic and functional gut microbiome profiles.

D. rotundus (sanguivorous, red), R. ferrumequinum (insectivorous, black), M. gigas (carnivorous, green), and R. aegyptiacus (frugivorous, blue). (A) Euclidean distance dendrogram of the microbial presence/absence identifications at the species taxonomical level. (B) Euclidean distance dendrogram from the Uniprot identified abundance functions from the normalized samples.

Figure 4. Traits in both the genome and gut microbiome with direct roles in the adaptation for sanguivory.

(A) GOs of the single copy orthologous genes with a dN/dS ratio that is statistically higher or lower in the common vampire bat in comparison to the other bats. (B) KEGG ontologies (KOs) from the common vampire bat gut microbiome functional core. (C) Genes with a dN/dS ratio that is statistically higher or lower in the common vampire bat in comparison to the other bats and that are directly associated to sanguivory challenges. (D) Taxa and genes from the common vampire bat gut microbiome core directly associated to the adaptation to sanguivory.