Genome analysis reveals insights into physiology and longevity of the Brandt's bat Myotis brandtii

Abstract

Bats account for one-fifth of mammalian species, are the only mammals with powered flight, and are among the few animals that echolocate. The insect-eating Brandt's bat (Myotis brandtii) is the longest-lived bat species known to date (lifespan exceeds 40 years) and, at 4-8 g adult body weight, is the most extreme mammal with regard to disparity between body mass and longevity. Here we report sequencing and analysis of the Brandt's bat genome and transcriptome, which suggest adaptations consistent with echolocation and hibernation, as well as altered metabolism, reproduction and visual function. Unique sequence changes in growth hormone and insulin-like growth factor 1 receptors are also observed. The data suggest that an altered growth hormone/insulin-like growth factor 1 axis, which may be common to other long-lived bat species, together with adaptations such as hibernation and low reproductive rate, contribute to the exceptional lifespan of the Brandt's bat.

Figure 1. Species map of M. brandtii.

(a) M. brandtii. (b) Occurrence of M. brandtii and areas of sample collection. Coloured dots indicate the location of sampled hibernating (December and April; shown in blue) and summer-active (June; shown in red) animals.

Figure 2. Relationship of M. brandtii to other mammals.

Consensus phylogenetic tree shows the relationship among nine mammals based on 2,654 single-copy genes. The divergence times for all nodes were estimated based on the four red nodes with fossil records as calibration times and marked in each node with error range. Gene family expansion events are marked in green, and gene family contraction events in red. MRCA refers to the gene family number of the most recent common ancestor.

Figure 3. FSHβ of the Brandt’s bat harbours a radical amino-acid substitution in a conserved position.

(a) Alignment of FSHB-encoded peptide sequences. Amino-acid numbering corresponds to the mature FSHβ peptide. (b) Structural model of FSHβ (cyan), the follicle-stimulating hormone receptor FSHR (grey) and the glycoprotein hormones α chain GLHA/FSHα (green) (PDB ID code 1xwd). In both subfigures, FSHβ residues buried at the FSHR receptor–ligand interface are highlighted in purple, while a radical amino-acid substitution within the interface in bats with delayed ovulation is shown in red.

Figure 4. Adaptations in the GH/IGF1 axis of the Brandt’s bat and its much longer lifespan than expected for its body size.

(a) Alignment of mammalian GHR protein sequences. An amino-acid deletion at position 284 and a methionine at position 275 unique to bats in the Vespertilionoidea superfamily are shown in red. Insect-eating bats are shown in blue and fruit-eating bats in orange. (b) Alignment of mammalian IGF1R protein sequences. Unique amino-acid replacements in bats in the Vespertilionoidea superfamily are highlighted in red. Identical residues and similar residues are shaded in black and grey, respectively. (c) Correlation between body mass and maximum lifespan in mammals. Myotis bats are shown as blue diamonds, and other mammals as grey circles. The Brandt’s bat is indicated by a red diamond.