Six new reference-quality bat genomes illuminate the molecular basis and evolution of bat adaptations
Graham M. Hughes,
Lars S Jermiin,
Emilia C Skirmuntt,
David Tech Ray,
Kevin A. M. Sullivan,
Juliana G. Roscito,
Bogdan M. Kirilenko,
Angelique P Corthals,
Megan L. Power,
Roger D Ransome,
Andrea G Locatelli,
Sebastien J. Puechmaille,
Erich D Jarvis,
Mark S. Springer,
Sonja C. Vernes,
Eugene W Myers,
Emma C. Teeling
Posted 09 Nov 2019
bioRxiv DOI: 10.1101/836874 (published DOI: 10.1038/s41586-020-2486-3)
Posted 09 Nov 2019
Bats account for ~20% of all extant mammal species and are considered exceptional given their extraordinary adaptations, including biosonar, true flight, extreme longevity, and unparalleled immune systems. To understand these adaptations, we generated reference-quality genomes of six species representing the key divergent lineages. We assembled these genomes with a novel pipeline incorporating state-of-the-art long-read and long-range sequencing and assembly techniques. The genomes were annotated using a maximal evidence approach, de novo predictions, protein/mRNA alignments, Iso-seq long read and RNA-seq short read transcripts, and gene projections from our new TOGA pipeline, retrieving virtually all (>99%) mammalian BUSCO genes. Phylogenetic analyses of 12,931 protein coding-genes and 10,857 conserved non-coding elements identified across 48 mammalian genomes helped to resolve bats' closest extant relatives within Laurasiatheria, supporting a basal position for bats within Scrotifera. Genome-wide screens along the bat ancestral branch revealed (a) selection on hearing-involved genes (e.g LRP2, SERPINB6, TJP2), which suggest that laryngeal echolocation is a shared ancestral trait of bats; (b) selection (e.g INAVA, CXCL13, NPSR1) and loss of immunity related proteins (e.g. LRRC70, IL36G), including pro-inflammatory NF-kB signalling; and (c) expansion of the APOBEC family, associated with restricting viral infection, transposon activity and interferon signalling. We also identified unique integrated viruses, indicating that bats have a history of tolerating viral pathogens, lethal to other mammal species. Non-coding RNA analyses identified variant and novel microRNAs, revealing regulatory relationships that may contribute to phenotypic diversity in bats. Together, our reference-quality genomes, high-quality annotations, genome-wide screens and in-vitro tests revealed previously unknown genomic adaptations in bats that may explain their extraordinary traits.
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