Chromosome-level Genome and Population Genomics of the Intermediate Horseshoe Bat ( Reveal the Molecular Basis of Virus Tolerance in and Echolocation Call Frequency Variation

Overview

Journal Zool Res

Publisher Science Press

Specialties Biology
Veterinary Medicine

Date 2024 Sep 11

PMID 39257377

Authors

Le Zhao

Jiaqing Yuan

Guiqiang Wang

Haohao Jing

Chen Huang

Lulu Xu

Xiao Xu

Ting Sun

Wu Chen

Xiuguang Mao

Gang Li

Affiliations

Soon will be listed here.

Abstract

Horseshoe bats (genus , family Rhinolophidae) represent an important group within chiropteran phylogeny due to their distinctive traits, including constant high-frequency echolocation, rapid karyotype evolution, and unique immune system. Advances in evolutionary biology, supported by high-quality reference genomes and comprehensive whole-genome data, have significantly enhanced our understanding of species origins, speciation mechanisms, adaptive evolutionary processes, and phenotypic diversity. However, genomic research and understanding of the evolutionary patterns of are severely constrained by limited data, with only a single published genome of currently available. In this study, we constructed a high-quality chromosome-level reference genome for the intermediate horseshoe bat ( ). Comparative genomic analyses revealed potential genetic characteristics associated with virus tolerance in Rhinolophidae. Notably, we observed expansions in several immune-related gene families and identified various genes functionally associated with the SARS-CoV-2 signaling pathway, DNA repair, and apoptosis, which displayed signs of rapid evolution. In addition, we observed an expansion of the major histocompatibility complex class II (MHC-II) region and a higher copy number of the - gene in horseshoe bats compared to other chiropteran species. Based on whole-genome resequencing and population genomic analyses, we identified multiple candidate loci (e.g., ) associated with variations in echolocation call frequency across subspecies. This research not only expands our understanding of the genetic characteristics of the genus but also establishes a valuable foundation for future research.

References

Traven A, Heierhorst J . SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. Bioessays. 2005; 27(4):397-407. DOI: 10.1002/bies.20204. View

Jacquet S, Culbertson M, Zhang C, El Filali A, De La Myre Mory C, Pons J . Adaptive duplication and genetic diversification of protein kinase R contribute to the specificity of bat-virus interactions. Sci Adv. 2022; 8(47):eadd7540. PMC: 9683710. DOI: 10.1126/sciadv.add7540. View

Wilkins M, Seddon N, Safran R . Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol. 2012; 28(3):156-66. DOI: 10.1016/j.tree.2012.10.002. View

Jebb D, Huang Z, Pippel M, Hughes G, Lavrichenko K, Devanna P . Six reference-quality genomes reveal evolution of bat adaptations. Nature. 2020; 583(7817):578-584. PMC: 8075899. DOI: 10.1038/s41586-020-2486-3. View

Mao X, Nie W, Wang J, Su W, Ao L, Feng Q . Karyotype evolution in Rhinolophus bats (Rhinolophidae, Chiroptera) illuminated by cross-species chromosome painting and G-banding comparison. Chromosome Res. 2007; 15(7):835-48. DOI: 10.1007/s10577-007-1167-5. View

Zhou P, Yang X, Wang X, Hu B, Zhang L, Zhang W . A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020; 579(7798):270-273. PMC: 7095418. DOI: 10.1038/s41586-020-2012-7. View

Wagner E, Shin J . Mechanisms of Hair Cell Damage and Repair. Trends Neurosci. 2019; 42(6):414-424. PMC: 6556399. DOI: 10.1016/j.tins.2019.03.006. View

Hayward J, Tachedjian M, Johnson A, Irving A, Gordon T, Cui J . Unique Evolution of Antiviral Tetherin in Bats. J Virol. 2022; 96(20):e0115222. PMC: 9599465. DOI: 10.1128/jvi.01152-22. View

Ruiz-Aravena M, McKee C, Gamble A, Lunn T, Morris A, Snedden C . Ecology, evolution and spillover of coronaviruses from bats. Nat Rev Microbiol. 2021; 20(5):299-314. PMC: 8603903. DOI: 10.1038/s41579-021-00652-2. View

10.

Habtemichael N, Heinrich U, Knauer S, Schmidtmann I, Bier C, Docter D . Expression analysis suggests a potential cytoprotective role of Birc5 in the inner ear. Mol Cell Neurosci. 2010; 45(3):297-305. DOI: 10.1016/j.mcn.2010.07.003. View

11.

Tian S, Zeng J, Jiao H, Zhang D, Zhang L, Lei C . Comparative analyses of bat genomes identify distinct evolution of immunity in Old World fruit bats. Sci Adv. 2023; 9(18):eadd0141. PMC: 10162675. DOI: 10.1126/sciadv.add0141. View

12.

Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B . AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006; 34(Web Server issue):W435-9. PMC: 1538822. DOI: 10.1093/nar/gkl200. View

13.

Jones G, Teeling E . The evolution of echolocation in bats. Trends Ecol Evol. 2006; 21(3):149-56. DOI: 10.1016/j.tree.2006.01.001. View

14.

Barcellos L, May S, Ramsay P, Quach H, Lane J, Nititham J . High-density SNP screening of the major histocompatibility complex in systemic lupus erythematosus demonstrates strong evidence for independent susceptibility regions. PLoS Genet. 2009; 5(10):e1000696. PMC: 2758598. DOI: 10.1371/journal.pgen.1000696. View

15.

Servedio M, van Doorn G, Kopp M, Frame A, Nosil P . Magic traits in speciation: 'magic' but not rare?. Trends Ecol Evol. 2011; 26(8):389-97. DOI: 10.1016/j.tree.2011.04.005. View

16.

Sai N, Yang Y, Ma L, Liu D, Jiang Q, Guo W . Involvement of NLRP3-inflammasome pathway in noise-induced hearing loss. Neural Regen Res. 2022; 17(12):2750-2754. PMC: 9165387. DOI: 10.4103/1673-5374.339499. View

17.

Sanderson M . r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics. 2003; 19(2):301-2. DOI: 10.1093/bioinformatics/19.2.301. View

18.

Ahn M, Cui J, Irving A, Wang L . Unique Loss of the PYHIN Gene Family in Bats Amongst Mammals: Implications for Inflammasome Sensing. Sci Rep. 2016; 6:21722. PMC: 4764838. DOI: 10.1038/srep21722. View

19.

Foley N, Springer M, Teeling E . Mammal madness: is the mammal tree of life not yet resolved?. Philos Trans R Soc Lond B Biol Sci. 2016; 371(1699). PMC: 4920340. DOI: 10.1098/rstb.2015.0140. View

20.

Dudchenko O, Batra S, Omer A, Nyquist S, Hoeger M, Durand N . De novo assembly of the genome using Hi-C yields chromosome-length scaffolds. Science. 2017; 356(6333):92-95. PMC: 5635820. DOI: 10.1126/science.aal3327. View