Six reference-quality genomes reveal evolution of bat adaptations

Abstract

Bats possess extraordinary adaptations, including flight, echolocation, extreme longevity and unique immunity. High-quality genomes are crucial for understanding the molecular basis and evolution of these traits. Here we incorporated long-read sequencing and state-of-the-art scaffolding protocols 1 to generate, to our knowledge, the first reference-quality genomes of six bat species (Rhinolophus ferrumequinum, Rousettus aegyptiacus, Phyllostomus discolor, Myotis myotis, Pipistrellus kuhlii and Molossus molossus). We integrated gene projections from our 'Tool to infer Orthologs from Genome Alignments' (TOGA) software with de novo and homology gene predictions as well as short-and long-read transcriptomics to generate highly complete gene annotations. To resolve the phylogenetic position of bats within Laurasiatheria, we applied several phylogenetic methods to comprehensive sets of orthologous protein-coding and noncoding regions of the genome, and identified a basal origin for bats within Scrotifera. Our genome-wide screens revealed positive selection on hearing-related genes in the ancestral branch of bats, which is indicative of laryngeal echolocation being an ancestral trait in this clade. We found selection and loss of immunity-related genes (including pro-inflammatory NF-κB regulators) and expansions of anti-viral APOBEC3 genes, which highlights molecular mechanisms that may contribute to the exceptional immunity of bats. Genomic integrations of diverse viruses provide a genomic record of historical tolerance to viral infection in bats. Finally, we found and experimentally validated bat-specific variation in microRNAs, which may regulate bat-specific gene-expression programs. Our reference-quality bat genomes provide the resources required to uncover and validate the genomic basis of adaptations of bats, and stimulate new avenues of research that are directly relevant to human health and disease 1. With more than 1,400 species identified to date 2 , bats (Chiroptera) account for about 20% of all extant mammal species. Bats are found around the world and successfully occupy diverse ecological niches 1. Their global success is attributed to an extraordinary suite of adaptations 1 including powered flight, laryngeal echolocation, vocal learning, exceptional longevity and a unique immune system that probably enables bats to better tolerate viruses that are lethal to other mammals (such as severe acute respiratory syndrome-related coronavirus, Middle East respiratory syndrome-related coronavirus and Ebola virus) 3. Bats therefore represent important model systems for the study of

SARS-CoV-2 variants evolved during the early stage of the pandemic and effects of mutations on adaptation in Wuhan populations

“…4) [51]. Previous studies have drawn on the increasing global database of annotated genomes of vertebrates, particularly new genomes provided by the Bat1K Collaboration, Zoonomia, and Vertebrate Genomes Project, associated with Genomes 10K-affiliated, as well as other sources [52,53]. A phylogenetic study of ACE2 orthologs from 410 vertebrates was performed.…”

Fundamental Characteristics of Bat Interferon Systems

“…Pteropodid bats are described as exhibiting a different amino acid within LRP2 and these bats do not have laryngeal echolocation. These results suggest that if these gene mutations are related to echolocation, then this would prove the origin of echolocation in bats with evidence for echolocation present in the bat ancestor that was subsequently lost in pteropodid bats (Jebb et al, 2020). More significantly to this review, the genome-wide screenings conducted by the Bat1K project also found that bat-specific selection had occurred on several genes that are related to immunity.…”

“…Through screening, they investigated gene loss, gain and selection to identify novel genes that are likely associated with viral tolerance within bats. These results will hence prove extremely useful in expanding existing knowledge of bat immunology within this fertile field of research (Jebb et al, 2020). Upon performing unbiased genome-wide screens for gene changes within the six bat species, Jebb et al (2020) identified nine genes that have undergone positive selection in the bat ancestor.…”

“…These results will hence prove extremely useful in expanding existing knowledge of bat immunology within this fertile field of research (Jebb et al, 2020). Upon performing unbiased genome-wide screens for gene changes within the six bat species, Jebb et al (2020) identified nine genes that have undergone positive selection in the bat ancestor. Among these are the genes LRP2 and SERPINB6 which have known roles in hearing.…”

Transcriptome sequencing of cochleae from constant-frequency and frequency-modulated echolocating bats

“…In addition, FL transcriptomes from FM bats and two CF subspecies could be used to test the roles of alternative splicing in the divergence of different echolocating types (CF and FM) and in intraspecific echolocation call frequency variation. Finally, these FL transcriptome datasets will be useful for identification of novel transcripts and for improvement of genome annotation of Rhinolophus affinis,Myotis ricketti, and other bat species 19,20 . Table 2.…”