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Volume 50 Issue 8
Aug.  2023
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Article Contents

Population genomic analysis reveals distinct demographics and recent adaptation in the black flying fox (Pteropus alecto)

doi: 10.1016/j.jgg.2023.05.002
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This work is supported in part by the National Natural Science Foundation of China (32293190, 32293192) and National Key R&D Program of China (2019YFA0709501). M.L. is supported in part by the National Natural Science Foundation of China (11971459). W.Z. is supported in part by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDPB17), the National Natural Science Foundation of China (31970566), and National Key R&D Program of China (2018YFC1406902 and 2018YFC0910400). The Duke-NUS team was supported in part by a grant from the Singapore National Research Foundation (NRFCRP10-2012-05).

  • Received Date: 2023-02-21
  • Revised Date: 2023-05-03
  • Accepted Date: 2023-05-03
  • Publish Date: 2023-05-12
  • As the only mammalian group capable of powered flight, bats have many unique biological traits. Previous comparative genomic studies in bats have focused on long-term evolution. However, the microevolutionary processes driving recent evolution are largely under-explored. Using resequencing data from 50 black flying foxes (Pteropus alecto), one of the model species for bats, we find that black flying fox has much higher genetic diversity and lower levels of linkage disequilibrium than most of the mammalian species. Demographic inference reveals strong population fluctuations (>100 fold) coinciding with multiple historical events including the last glacial change and Toba super eruption, suggesting that the black flying fox is a very resilient species with strong recovery abilities. While long-term adaptation in the black flying fox is enriched in metabolic genes, recent adaptation in the black flying fox has a unique landscape where recently selected genes are not strongly enriched in any functional category. The demographic history and mode of adaptation suggest that black flying fox might be a well-adapted species with strong evolutionary resilience. Taken together, this study unravels a vibrant landscape of recent evolution for the black flying fox and sheds light on several unique evolutionary processes for bats comparing to other mammalian groups.
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  • Alexander, D.H., Novembre, J., Lange, K., 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664.
    Altringham, J.D., 2011. Bats:from Evolution to Conservation. Oxford University Press. Auton, A., Rui Li, Y., Kidd, J., Oliveira, K., Nadel, J., Holloway, J.K., Hayward, J.J., Cohen, P.E., Greally, J.M., Wang, J., 2013. Genetic recombination is targeted towards gene promoter regions in dogs. PLoS Genet. 9, e1003984.
    Bergeron, L.A., Besenbacher, S., Zheng, J., Li, P., Bertelsen, M.F., Quintard, B., Hoffman, J.I., Li, Z., St. Leger, J., Shao, C., et al., 2023. Evolution of the germline mutation rate across vertebrates. Nature 615, 285-291.
    Browning, B.L., Zhou, Y., Browning, S.R., 2018. A one-penny imputed genome from next-generation reference panels. Am. J. Hum. Genet. 103, 338-348.
    Bu, D., Luo, H., Huo, P., Wang, Z., Zhang, S., He, Z., Wu, Y., Zhao, L., Liu, J., Guo, J., et al., 2021. KOBAS-i:intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Res. 49, W317eW325.
    Buggiotti, L., Yurchenko, A.A., Yudin, N.S., Vander Jagt, C.J., Vorobieva, N.V., Kusliy, M.A., Vasiliev, S.K., Rodionov, A.N., Boronetskaya, O.I., Zinovieva, N.A., et al., 2021. Demographic history, adaptation, and NRAP convergent evolution at amino acid residue 100 in the world northernmost cattle from Siberia. Mol. Biol. Evol. 38, 3093-3110.
    Cho, Y.S., Hu, L., Hou, H., Lee, H., Xu, J., Kwon, S., Oh, S., Kim, H.-M., Jho, S., Kim, S., et al., 2013. The tiger genome and comparative analysis with lion and snow leopard genomes. Nat. Commun. 4, 2433.
    Consortium, Z., 2020. A comparative genomics multitool for scientific discovery and conservation. Nature 587, 240-245.
    Crisci, J.L., Poh, Y.-P., Mahajan, S., Jensen, J.D., 2013. The impact of equilibrium assumptions on tests of selection. Front. Genet. 4, 235.
    Danecek, P., Auton, A., Abecasis, G., Albers, C.A., Banks, E., DePristo, M.A., Handsaker, R.E., Lunter, G., Marth, G.T., Sherry, S.T., et al., 2011. The variant call format and VCFtools. Bioinformatics 27, 2156-2158.
    DeGiorgio, M., Huber, C.D., Hubisz, M.J., Hellmann, I., Nielsen, R., 2016. SweepFinder2:increased sensitivity, robustness and flexibility. Bioinformatics 32, 1895-1897.
    Dennis, G., Sherman, B.T., Hosack, D.A., Yang, J., Gao, W., Lane, H.C., Lempicki, R.A., 2003. DAVID:database for annotation, visualization, and integrated discovery. Genome Biol. 4, R60.
    Dong, D., Lei, M., Hua, P., Pan, Y.-H., Mu, S., Zheng, G., Pang, E., Lin, K., Zhang, S., 2017. The genomes of two bat species with long constant frequency echolocation calls. Mol. Biol. Evol. 34, 20-34.
    Eaton, B.T., Broder, C.C., Middleton, D., Wang, L.-F., 2006. Hendra and Nipah viruses:different and dangerous. Nat. Rev. Microbiol. 4, 23-35.
    Eilertson, K.E., Booth, J.G., Bustamante, C.D., 2012. SnIPRE:selection inference using a Poisson random effects model. PLoS Comput. Biol. 8, e1002806.
    Fairley, S., Lowy-Gallego, E., Perry, E., Flicek, P., 2020. The International Genome Sample Resource (IGSR) collection of open human genomic variation resources. Nucleic Acids Res. 48, D941eD947.
    Fraser, G.C., Hooper, P.T., Lunt, R.A., Gould, A.R., Gleeson, L.J., Hyatt, A.D., Russell, G.M., Kattenbelt, J.A., 1996. Encephalitis caused by a Lyssavirus in fruit bats in Australia. Emerg. Infect. Dis. 2, 327.
    Guan, D., McCarthy, S.A., Wood, J., Howe, K., Wang, Y., Durbin, R., 2020. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36, 2896-2898.
    Hall, A.B., Qi, Y., Timoshevskiy, V., Sharakhova, M.V., Sharakhov, I.V., Tu, Z., 2013. Six novel Y chromosome genes in Anopheles mosquitoes discovered by independently sequencing males and females. BMC Genomics 14, 273.
    Hall, L.S., Richards, G., 2000. Flying Foxes:Fruit and Blossom Bats of Australia. UNSW Press.
    Halpin, K., Young, P.L., Field, H., Mackenzie, J., 2000. Isolation of Hendra virus from pteropid bats:a natural reservoir of Hendra virus. J. Gen. Virol. 81, 1927-1932.
    Hansen, J., Sato, M., Russell, G., Kharecha, P., 2013. Climate sensitivity, sea level and atmospheric carbon dioxide. Philos. Trans. R. Soc. A 371, 20120294.
    Hawkins, J.A., Kaczmarek, M.E., Mü ller, M.A., Drosten, C., Press, W.H., Sawyer, S.L., 2019. A metaanalysis of bat phylogenetics and positive selection based on genomes and transcriptomes from 18 species. Proc. Natl. Acad. Sci. U. S. A. 116, 11351-11360.
    Hu, B., Zeng, L.-P., Yang, X.-L., Ge, X.-Y., Zhang, W., Li, B., Xie, J.-Z., Shen, X.-R., Zhang, Y.-Z., Wang, N., et al., 2017. Discovery of a rich gene pool of bat SARSrelated coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathog. 13, e1006698.
    Hudson, R.R., 2002. Generating samples under a WrighteFisher neutral model of genetic variation. Bioinformatics 18, 337-338.
    Hung, C.-M., Shaner, P.-J.L., Zink, R.M., Liu, W.-C., Chu, T.-C., Huang, W.-S., Li, S.-H., 2014. Drastic population fluctuations explain the rapid extinction of the passenger pigeon. Proc. Natl. Acad. Sci. U. S. A. 111, 10636-10641.
    Iannucci, A., Benazzo, A., Natali, C., Arida, E.A., Zein, M.S.A., Jessop, T.S., Bertorelle, G., Ciofi, C., 2021. Population structure, genomic diversity and demographic history of Komodo dragons inferred from whole-genome sequencing. Mol. Ecol. 30, 6309-6324.
    Jebb, D., Huang, Z., Pippel, M., Hughes, G.M., Lavrichenko, K., Devanna, P., Winkler, S., Jermiin, L.S., Skirmuntt, E.C., Katzourakis, A., et al., 2020. Six reference-quality genomes reveal evolution of bat adaptations. Nature 583, 578-584.
    Johnson, R.N., O'Meally, D., Chen, Z., Etherington, G.J., Ho, S.Y., Nash, W.J., Grueber, C.E., Cheng, Y., Whittington, C.M., Dennison, S., et al., 2018. Adaptation and conservation insights from the koala genome. Nat. Genet. 50, 1102-1111.
    Kumar, S., Subramanian, S., 2002. Mutation rates in mammalian genomes. Proc. Natl. Acad. Sci. U. S. A. 99, 803-808.
    Kunz, T.H., Fenton, M.B., 2005. Bat Ecology. University of Chicago Press.
    Larson, G., Fuller, D.Q., 2014. The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 45, 115-136.
    Li, H., Durbin, R., 2009. Fast and accurate short read alignment with BurrowseWheeler transform. Bioinformatics 25, 1754-1760.
    Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079.
    Liu, X., Fu, Y.-X., 2020. Stairway Plot 2:demographic history inference with folded SNP frequency spectra. Genome Biol. 21, 280.
    Manichaikul, A., Mychaleckyj, J.C., Rich, S.S., Daly, K., Sale, M., Chen, W.-M., 2010. Robust relationship inference in genome-wide association studies. Bioinformatics 26, 2867-2873.
    Martin, P.S., Klein, R.G., 2022. Quaternary Extinctions:a Prehistoric Revolution. University of Arizona Press.
    Mather, K.A., Caicedo, A.L., Polato, N.R., Olsen, K.M., McCouch, S., Purugganan, M.D., 2007. The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177, 2223-2232.
    McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al., 2010. The Genome Analysis Toolkit:a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.
    Mickleburgh, S.P., Hutson, A.M., Racey, P.A., 1992. Old world fruit bats:an action plan for their conservation. https://doi.org/10.2305/IUCN.CH.1992.SSC-AP.6.en.
    Nater, A., Nietlisbach, P., Arora, N., van Schaik, C.P., van Noordwijk, M.A., Willems, E.P., Singleton, I., Wich, S.A., Goossens, B., Warren, K.S., et al., 2011. Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant orangutans (genus:Pongo). Mol. Biol. Evol. 28, 2275-2288.
    Nelson, C.W., Moncla, L.H., Hughes, A.L., 2015. SNPGenie:estimating evolutionary parameters to detect natural selection using pooled next-generation sequencing data. Bioinformatics 31, 3709-3711.
    Nikaido, M., Kondo, S., Zhang, Z., Wu, J., Nishihara, H., Niimura, Y., Suzuki, S., Touhara, K., Suzuki, Y., Noguchi, H., 2020. Comparative genomic analyses illuminate the distinct evolution of megabats within Chiroptera. DNA Res. 27, dsaa021.
    O'Connell, K.A., Oaks, J.R., Hamidy, A., Shaney, K.J., Kurniawan, N., Smith, E.N., Fujita, M.K., 2020. Impacts of the Toba eruption and montane forest expansion on diversification in Sumatran parachuting frogs (Rhacophorus). Mol. Ecol. 29, 2994-3009.
    Palmer, C., Price, O., Bach, C., 2000. Foraging ecology of the black flying fox(Pteropus alecto) in the seasonal tropics of the Northern Territory, Australia. Wildlife Res. 27, 169-178.
    Palmer, C., Woinarski, J., 1999. Seasonal roosts and foraging movements of the black flying fox (Pteropus alecto) in the Northern Territory:resource tracking in a landscape mosaic. Wildlife Res. 26, 823-838.
    Parker, J., Tsagkogeorga, G., Cotton, J.A., Liu, Y., Provero, P., Stupka, E., Rossiter, S.J., 2013. Genome-wide signatures of convergent evolution in echolocating mammals. Nature 502, 228-231.
    Pavlovich, S.S., Lovett, S.P., Koroleva, G., Guito, J.C., Arnold, C.E., Nagle, E.R., Kulcsar, K., Lee, A., Thibaud-Nissen, F., Hume, A.J., et al., 2018. The Egyptian rousette genome reveals unexpected features of bat antiviral immunity. Cell 173, 1098-1110.
    Pierson, E.D., Rainey, W.E., 1992. The biology of flying foxes of the genus Pteropus:a review. In:Paper Presented at:Pacific Island Flying Foxes:Proceedings of an International Conservation Conference US Department of the Interior Fish and Wildlife Service, Washington, DC.
    Price, A.L., Patterson, N.J., Plenge, R.M., Weinblatt, M.E., Shadick, N.A., Reich, D., 2006. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904-909.
    Qiu, Q., Zhang, G., Ma, T., Qian, W., Wang, J., Ye, Z., Cao, C., Hu, Q., Kim, J., Larkin, D.M., et al., 2012. The yak genome and adaptation to life at high altitude. Nat. Genet. 44, 946-949.
    Qu, Y., Zhao, H., Han, N., Zhou, G., Song, G., Gao, B., Tian, S., Zhang, J., Zhang, R., Meng, X., et al., 2013. Ground tit genome reveals avian adaptation to living at high altitudes in the Tibetan plateau. Nat. Commun. 4, 2071.
    Rohatgi, A., 2022. WebPlotDigitizer:Version 4.6. https://automeris.io/WebPlotDigitizer.
    Rose, W.I., Chesner, C.A., 1990. Worldwide dispersal of ash and gases from earth's largest known eruption:Toba, Sumatra, 75 ka. Glob. Planet. Change 89, 269-275.
    Santillan, D.D.M., Lama, T.M., Guerrero, Y.T.G., Brown, A.M., Donat, P., Zhao, H., Rossiter, S.J., Yohe, L.R., Potter, J.H., Teeling, E.C., et al., 2021. Large-scale genome sampling reveals unique immunity and metabolic adaptations in bats. Mol. Ecol. 30, 6449-6467.
    Seim, I., Fang, X., Xiong, Z., Lobanov, A.V., Huang, Z., Ma, S., Feng, Y., Turanov, A.A., Zhu, Y., Lenz, T.L., et al., 2013. Genome analysis reveals insights into physiology and longevity of the Brandt's bat Myotis brandtii. Nat. Commun. 4, 2212.
    Sella, G., Petrov, D.A., Przeworski, M., Andolfatto, P., 2009. Pervasive natural selection in the Drosophila genome? PLoS Genet. 5, e1000495.
    Shen, Y.-Y., Liang, L., Zhu, Z.-H., Zhou, W.-P., Irwin, D.M., Zhang, Y.-P., 2010. Adaptive evolution of energy metabolism genes and the origin of flight in bats. Proc. Natl. Acad. Sci. U. S. A. 107, 8666-8671.
    Smith, E.I., Jacobs, Z., Johnsen, R., Ren, M., Fisher, E.C., Oestmo, S., Wilkins, J., Harris, J.A., Karkanas, P., Fitch, S., et al., 2018. Humans thrived in South Africa through the Toba eruption about 74,000 years ago. Nature 555, 511-515.
    Smith, A.V., Thomas, D.J., Munro, H.M., Abecasis, G.R., 2005. Sequence features in regions of weak and strong linkage disequilibrium. Genome Res. 15, 1519-1534.
    Spence, J.P., Song, Y.S., 2019. Inference and analysis of population-specific finescale recombination maps across 26 diverse human populations. Sci. Adv. 5, eaaw9206.
    Springer, M.S., Teeling, E.C., Madsen, O., Stanhope, M.J., de Jong, W.W., 2001. Integrated fossil and molecular data reconstruct bat echolocation. Proc. Natl. Acad. Sci. U. S. A. 98, 6241-6246.
    Szpiech, Z.A., 2021. Selscan 2.0:scanning for sweeps in unphased data. bioRxiv. https://doi.org/10.1101/2021.10.22.465497.
    Szpiech, Z.A., Hernandez, R.D., 2014. selscan:an efficient multithreaded program to perform EHH-based scans for positive selection. Mol. Biol. Evol. 31, 2824-2827.
    Tang, B., Zhou, Q., Dong, L., Li, W., Zhang, X., Lan, L., Zhai, S., Xiao, J., Zhang, Z., Bao, Y., et al., 2019. iDog:an integrated resource for domestic dogs and wild canids. Nucleic Acids Res. 47, D793eD800.
    Teeling, E.C., Springer, M.S., Madsen, O., Bates, P., O'brien, S.J., Murphy, W.J., 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307, 580-584.
    Teeling, E.C., Vernes, S.C., Davalos, L.M., Ray, D.A., Gilbert, M.T.P., Myers, E., Consortium, B.K., 2018. Bat biology, genomes, and the Bat1K project:to generate chromosome-level genomes for all living bat species. Annu. Rev. Anim. Biosci. 6, 23-46.
    Teng, H., Zhang, Y., Shi, C., Mao, F., Cai, W., Lu, L., Zhao, F., Sun, Z., Zhang, J., 2017. Population genomics reveals speciation and introgression between brown Norway rats and their sibling species. Mol. Biol. Evol. 34, 2214-2228.
    Tian, R., Han, K., Geng, Y., Yang, C., Shi, C., Thomas, P.B., Pearce, C., Moffatt, K., Ma, S., Xu, S., et al., 2022. A chromosome-level genome of Antechinus flavipes provides a reference for an Australian marsupial genus with male death after mating. Mol. Ecol. Resour. 22, 740-754.
    Van der Auwera, G.A., O'Connor, B.D., 2020. Genomics in the Cloud:Using Docker, GATK, and WDL in Terra. O'Reilly Media.
    Van Der Kaars, S., Miller, G.H., Turney, C.S., Cook, E.J., Nürnberg, D., Schonfeld, J., Kershaw, A.P., Lehman, S.J., 2017. Humans rather than climate the primary cause of Pleistocene megafaunal extinction in Australia. Nat. Commun. 8, 14142.
    Vicoso, B., Bachtrog, D., 2015. Numerous transitions of sex chromosomes in Diptera. PLoS Biol. 13, e1002078.
    Wang, K., Tian, S., Galindo-Gonzalez, J., D avalos, L.M., Zhang, Y., Zhao, H., 2020. Molecular adaptation and convergent evolution of frugivory in Old World and neotropical fruit bats. Mol. Ecol. 29, 4366-4381.
    Wang, L.-F., Walker, P.J., Poon, L.L., 2011. Mass extinctions, biodiversity and mitochondrial function:Are bats 'special'as reservoirs for emerging viruses? Curr. Opin. Virol. 1, 649-657.
    Webb, N., Tidemann, C., 1995. Hybridisation between black (Pteropods alecto) and grey-headed (P. poliocephalus) flying-foxes (Megachiroptera:Pteropodidae). Aust. Mammal. 18, 19-26.
    Webb, N., Tidemann, C., 1996. Mobility of Australian flying-foxes, Pteropus spp.(Megachiroptera):evidence from genetic variation. Proc. R. Soc. B-Biol. Sci. 263, 497-502.
    Wen, M., Ng, J.H., Zhu, F., Chionh, Y.T., Chia, W.N., Mendenhall, I.H., Lee, B.P.-H., Irving, A.T., Wang, L.-F., 2018. Exploring the genome and transcriptome of the cave nectar bat Eonycteris spelaea with PacBio long-read sequencing. Gigascience 7, giy116.
    Williams, M., 2012. The~73 ka Toba super-eruption and its impact:history of a debate. Quat. Int. 258, 19-29.
    Wu, T., Hu, E., Xu, S., Chen, M., Guo, P., Dai, Z., Feng, T., Zhou, L., Tang, W., Zhan, L., et al., 2021. clusterProfiler 4.0:a universal enrichment tool for interpreting omics data. Innovation 2, 100141.
    Yi, X., Liang, Y., Huerta-Sanchez, E., Jin, X., Cuo, Z.X.P., Pool, J.E., Xu, X., Jiang, H., Vinckenbosch, N., Korneliussen, T.S., et al., 2010. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329, 75-78.
    Zhang, G., Cowled, C., Shi, Z., Huang, Z., Bishop-Lilly, K.A., Fang, X., Wynne, J.W., Xiong, Z., Baker, M.L., Zhao, W., et al., 2013. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339, 456-460.
    Zhang, C., Dong, S.-S., Xu, J.-Y., He, W.-M., Yang, T.-L., 2019. PopLDdecay:a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35, 1786-1788.
    Zepeda Mendoza, M.L., Xiong, Z., Escalera-Zamudio, M., Runge, A.K., Thez e, J., Streicker, D., Frank, H.K., Loza-Rubio, E., Liu, S., Ryder, O.A., et al., 2018. Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat. Nat. Ecol. Evol. 2, 659-668.
    Zhou, H., Chen, X., Hu, T., Li, J., Song, H., Liu, Y., Wang, P., Liu, D., Yang, J., Holmes, E.C., et al., 2020. A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1/S2 cleavage site of the spike protein. Curr. Biol. 30, 2196-2203.
    Zubaid, A., McCracken, G.M., McCracken, G.F., Kunz, T.H., Kunz, T., 2006. Functional and Evolutionary Ecology of Bats. Oxford University Press.
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