Novel de Novo Genome of Cynopterus brachyotis Reveals Evolutionarily Abrupt Shifts in Gene Family Composition across Fruit Bats

Abstract

Major novel physiological or phenotypic adaptations often require accompanying modifications at the genic level. Conversely, the detection of considerable contractions and/or expansions of gene families can be an indicator of fundamental but unrecognized physiological change. We sequenced a novel fruit bat genome (Cynopterus brachyotis) and adopted a comparative approach to reconstruct the evolution of fruit bats, mapping contractions and expansions of gene families along their evolutionary history. Despite a radical change in life history as compared with other bats (e.g., loss of echolocation, large size, and frugivory), fruit bats have undergone surprisingly limited change in their genic composition, perhaps apart from a potentially novel gene family expansion relating to telomere protection and longevity. In sharp contrast, within fruit bats, the new Cynopterus genome bears the signal of unusual gene loss and gene family contraction, despite its similar morphology and lifestyle to two other major fruit bat lineages. Most missing genes are regulatory, immune-related, and olfactory in nature, illustrating the diversity of genomic strategies employed by bats to contend with responses to viral infection and olfactory requirements. Our results underscore that significant fluctuations in gene family composition are not always associated with obvious examples of novel physiological and phenotypic adaptations but may often relate to less-obvious shifts in immune strategies.

Lessons from the host defences of bats, a unique viral reservoir

“…These observations have triggered increasing efforts to study how bats limit excessive or aberrant innate immunue responses. From the initial characterization of two divergent bat genomes 83 and through more recent genome additions 73,116,117 , a consistent trend for the evolution of immune-related genes-including those encoding the pattern recognition receptors-has been revealed. Pattern recognition receptors sense endogenous molecules from damaged cells and structurally conserved microbial structures, known as damage and pathogen-associated molecular patterns, respectively 118 .…”

Comparative analyses of bat genomes identify distinct evolution of immunity in Old World fruit bats

“…We undertook comparative genomic analysis using our dataset of 18 focal mammals (data S1). For this, we performed gene prediction for our new C. sphinx genome as well as for the six chromosome-level bat genomes ( 15 ) and the Old World fruit bats Cynopterus brachyotis ( 19 ) and Macroglossus sobrinus [National Center for Biotechnology Information (NCBI) accession no. GCA_004027375.1] (data S1 and tables S14 to S16).…”

“…This species is widely distributed across South and Southeast Asia and is reported to host several β-coronaviruses ( 28 , 29 )—a group that includes MERS-CoV, SARS-CoV, and SARS-CoV-2 ( 30 ). By combining our newly generated genome with high-quality genome assemblies from five other pteropodid bats ( 15 , 19 ), related bats, and mammalian outgroups, we seek to determine whether pteropodid-specific modifications can explain variation in viral load ( 31 ).…”

A comparative study of RNA yields from museum specimens, including an optimized protocol for extracting RNA from formalin-fixed specimens

“…Reads were also mapped to reference transcriptomes when available using Bowtie2. For samples in the family Pteropodidae, reads were mapped to the Cynopterus brachyotis genome (GCA_009793145.1; Chattopadhyay et al, 2020) and the Rousettus aegyptiacus genome and transcriptome (GCF_014176215.1; Jebb et al, 2020). For samples in the genus Hipposideros, reads were mapped to the reference genome and transcriptome of Hipposideros armiger (GCF_001890085.1; Dong et al, 2017).…”