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Birth-and-death evolution of ribonuclease 9 genes in Cetartiodactyla

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Abstract

RNase9 plays a reproductive function and has been recognized as an important member of the ribonuclease (RNase) A superfamily, a gene family that is widely used as a model for molecular evolutionary studies. Here, we identified 178 RNase9 genes from 95 Cetartiodactyla species that represent all four lineages and 21 families of this clade. Unexpectedly, RNase9 experienced an evolutionary scenario of “birth and death” in Ruminantia, and expression analyses showed that duplicated RNase9A and RNase9B genes are expressed in reproductive tissues (epididymis, vas deferens or prostate). This expression pattern combined with the estimate that these genes duplicated during the middle Eocene, a time when Ruminantia become a successful lineage, suggests that the RNase9 gene duplication might have been advantageous for promoting sperm motility and male fertility as an adaptation to climate seasonality changes of this period. In contrast, all RNase9 genes were lost in the Cetacean lineage, which might be associated with their high levels of prostatic lesions and lower reproductive rates as adaptations to a fully aquatic environment and a balance to the demands of ocean resources. This study reveals a complex and intriguing evolutionary history and functional divergence for RNase9 in Cetartiodactyla, providing new insights into the evolution of the RNaseA superfamily and molecular mechanisms for organismal adaptations to the environment.

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References

  • Agustı, J., Siria, A.S., and Garcés, M. (2003). Explaining the end of the hominoid experiment in Europe. J Hum Evol 45, 145–153.

    Article  PubMed  Google Scholar 

  • Bian, C., Huang, Y., Li, J., You, X., Yi, Y., Ge, W., and Shi, Q. (2019). Divergence, evolution and adaptation in ray-finned fish genomes. Sci China Life Sci 62, 1003–1018.

    Article  PubMed  Google Scholar 

  • Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Gallo Cassarino, T., Bertoni, M., Bordoli, L., et al. (2014). SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42, W252–W258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bjellqvist, B., Basse, B., Olsen, E., and Celis, J.E. (1994). Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15, 529–539.

    Article  CAS  PubMed  Google Scholar 

  • Bordoli, L., and Schwede, T. (2012). Automated protein structure modeling with SWISS-MODEL Workspace and the Protein Model Portal. Methods Mol Biol 857, 107–136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cascieri, M., Amann, R.P., and Hammerstedt, R.H. (1976). Adenine nucleotide changes at initiation of bull sperm motility. J Biol Chem 251, 787–793.

    Article  CAS  PubMed  Google Scholar 

  • Castella, S., Fouchécourt, S., Teixeira-Gomes, A.P., Vinh, J., Belghazi, M., Dacheux, F., and Dacheux, J.L. (2004). Identification of a member of a new RNase A family specifically secreted by epididymal caput epithelium. Biol Reprod 70, 319–328.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, G.Z., Li, J.Y., Li, F., Wang, H.Y., and Shi, G.X. (2009). Human ribonuclease 9, a member of ribonuclease A superfamily, specifically expressed in epididymis, is a novel sperm-binding protein. Asian J Androl 11, 240–251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho, S., Beintema, J.J., and Zhang, J. (2005). The ribonuclease A superfamily of mammals and birds: identifying new members and tracing evolutionary histories. Genomics 85, 208–220.

    Article  CAS  PubMed  Google Scholar 

  • Cho, S., and Zhang, J. (2006). Ancient expansion of the ribonuclease A superfamily revealed by genomic analysis of placental and marsupial mammals. Gene 373, 116–125.

    Article  CAS  PubMed  Google Scholar 

  • Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9, 772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David, I., Kohnke, P., Lagriffoul, G., Praud, O., Plouarboué, F., Degond, P., and Druart, X. (2015). Mass sperm motility is associated with fertility in sheep. anim Reprod Sci 161, 75–81.

    Article  PubMed  Google Scholar 

  • Decker, J.E., Pires, J.C., Conant, G.C., McKay, S.D., Heaton, M.P., Chen, K., Cooper, A., Vilkki, J., Seabury, C.M., Caetano, A.R., et al. (2009). Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proc Natl Acad Sci USA 106, 18644–18649.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forde, N., and Lonergan, P. (2017). Interferon-tau and fertility in ruminants. Reproduction 154, F33–F43.

    Article  CAS  PubMed  Google Scholar 

  • Goo, S.M., and Cho, S. (2013). The expansion and functional diversification of the mammalian ribonuclease a superfamily epitomizes the efficiency of multigene families at generating biological novelty. Genome Biol Evol 5, 2124–2140.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu, X., Zou, Y., Su, Z., Huang, W., Zhou, Z., Arendsee, Z., and Zeng, Y. (2013). An update of DIVERGE software for functional divergence analysis of protein family. Mol Biol Evol 30, 1713–1719.

    Article  CAS  PubMed  Google Scholar 

  • Hassanin, A., Delsuc, F., Ropiquet, A., Hammer, C., Jansen van Vuuren, B., Matthee, C., Ruiz-Garcia, M., Catzeflis, F., Areskoug, V., Nguyen, T.T., et al. (2012). Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. Comptes Rendus Biol 335, 32–50.

    Article  Google Scholar 

  • Hebert, J., Lust, A., Fuller, A., Maloney, S.K., Mitchell, D., and Mitchell, G. (2008). Thermoregulation in pronghorn antelope (Antilocapra americana, Ord) in winter. J Exp Biol 211, 749–756.

    Article  CAS  PubMed  Google Scholar 

  • Huelsmann, M., Hecker, N., Springer, M.S., Gatesy, J., Sharma, V., and Hiller, M. (2019). Genes lost during the transition from land to water in cetaceans highlight genomic changes associated with aquatic adaptations. Sci Adv 5, eaaw6671.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janis, C. (1976). The evolutionary strategy of the equidae and the origins of rumen and cecal digestion. Evolution 30, 757–774.

    Article  PubMed  Google Scholar 

  • Jones, R.C., and Murdoch, R.N. (1996). Regulation of the motility and metabolism of spermatozoa for storage in the epididymis of eutherian and marsupial mammals. Reprod Fertil Dev 8, 553–568.

    Article  CAS  PubMed  Google Scholar 

  • Karniski, C., Krzyszczyk, E., and Mann, J. (2018). Senescence impacts reproduction and maternal investment in bottlenose dolphins. Proc R Soc B 285, 20181123.

    Article  PubMed  PubMed Central  Google Scholar 

  • Krutskikh, A., De Gendt, K., Sharp, V., Verhoeven, G., Poutanen, M., and Huhtaniemi, I. (2011). Targeted inactivation of the androgen receptor gene in murine proximal epididymis causes epithelial hypotrophy and obstructive azoospermia. Endocrinology 152, 689–696.

    Article  CAS  PubMed  Google Scholar 

  • Krutskikh, A., Poliandri, A., Cabrera-Sharp, V., Dacheux, J.L., Poutanen, M., and Huhtaniemi, I. (2012). Epididymal protein Rnase10 is required for post-testicular sperm maturation and male fertility. FASEB J 26, 4198–4209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lang, D., Lim, B.K., Gao, Y., and Wang, X. (2019). Adaptive evolutionary expansion of the ribonuclease 6 in Rodentia. Integr Zool 14, 306–317.

    Article  PubMed  Google Scholar 

  • Lang, D.T., Wang, X.P., Wang, L., and Yu, L. (2017). Molecular evolution of pancreatic ribonuclease gene (RNase1) in Rodentia. J Genet Genomics 44, 219–222.

    Article  PubMed  Google Scholar 

  • Li, H., and Durbin, R. (2010). Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589–595.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lill, M.A., and Danielson, M.L. (2011). Computer-aided drug design platform using PyMOL. J Comput Aided Mol Des 25, 13–19.

    Article  CAS  PubMed  Google Scholar 

  • Liu, G., Cui, X., Li, H., and Cai, L. (2016). Evolutionary direction of processed pseudogenes. Sci China Life Sci 59, 839–849.

    Article  CAS  PubMed  Google Scholar 

  • Liu, J., Wang, X.P., Cho, S., Lim, B.K., Irwin, D.M., Ryder, O.A., Zhang, Y.P., and Yu, L. (2014a). Evolutionary and functional novelty of pancreatic ribonuclease: a study of Musteloidea (order Carnivora). Sci Rep 4, 5070.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Y., He, G., Xu, H., Han, X., Jones, G., Rossiter, S.J., and Zhang, S. (2014b). Adaptive functional diversification of lysozyme in insectivorous bats. Mol Biol Evol 31, 2829–2835.

    Article  CAS  PubMed  Google Scholar 

  • Lust, A., Fuller, A., Maloney, S.K., Mitchell, D., and Mitchell, G. (2007). Thermoregulation in pronghorn antelope (Antilocapra americana Ord) in the summer. J Exp Biol 210, 2444–2452.

    Article  CAS  PubMed  Google Scholar 

  • Malo, A.F., Garde, J.J., Soler, A.J., Garcia, A..J., Gomendio, M., and Roldan, E.R.S. (2005). Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol Reprod 72, 822–829.

    Article  CAS  PubMed  Google Scholar 

  • Meredith, R.W., Janečka, J.E., Gatesy, J., Ryder, O.A., Fisher, C.A., Teeling, E.C., Goodbla, A., Eizirik, E., Simão, T.L.L., Stadler, T., et al. (2011). Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334, 521–524.

    Article  CAS  PubMed  Google Scholar 

  • Mitchell, G., and Lust, A. (2008). The carotid rete and artiodactyl success. Biol Lett 4, 415–418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mosbrugger, V., Utescher, T., and Dilcher, D.L. (2005). Cenozoic continental climatic evolution of Central Europe. Proc Natl Acad Sci USA 102, 14964–14969.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen, R., and Yang, Z. (1998). Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148, 929–936.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penttinen, J., Pujianto, D.A., Sipila, P., Huhtaniemi, I., and Poutanen, M. (2003). Discovery in silico and characterization in vitro of novel genes exclusively expressed in the mouse epididymis. Mol Endocrinol 17, 2138–2151.

    Article  CAS  PubMed  Google Scholar 

  • Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8, 785–786.

    Article  CAS  PubMed  Google Scholar 

  • Pomeroy, P. (2011). Reproductive cycles of marine mammals. Anim Reprod Sci 124, 184–193.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D., and Buckley, T.R. (2004). Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Systatic Biol 53, 793–808.

    Article  Google Scholar 

  • Rambaut, A., Drummond, A.J., Xie, D., Baele, G., and Suchard, M.A. (2018). Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 67, 901–904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., and Huelsenbeck, J.P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61, 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Santorum, J.M., Darriba, D., Taboada, G.L., and Posada, D. (2014). jmodeltest.org: selection of nucleotide substitution models on the cloud. Bioinformatics 30, 1310–1311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma, V., Hecker, N., Roscito, J.G., Foerster, L., Langer, B.E., and Hiller, M. (2018). A genomics approach reveals insights into the importance of gene losses for mammalian adaptations. Nat Commun 9, 1215.s.

    Article  Google Scholar 

  • Sharma, V., Schwede, P., and Hiller, M. (2017). CESAR 2.0 substantially improves speed and accuracy of comparative gene annotation. Bioinformatics 33, 3985–3987.

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Systatic Biol 57, 758–771.

    Article  Google Scholar 

  • Su, A.I., Wiltshire, T., Batalov, S., Lapp, H., Ching, K.A., Block, D., Zhang, J., Soden, R., Hayakawa, M., Kreiman, G., et al. (2004). A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101, 6062–6067.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suárez-Santana, C.M., Fernández, A., Sierra, E., Arbelo, M., Bernaldo de Quirós, Y., Andrada, M., Mompeo, B., Pérez, L., Blanco, A., Méndez, A., et al. (2020). Comparative morphology, histology, and cytology of odontocete cetaceans prostates. Anat Rec 303, 2036–2053.

    Article  Google Scholar 

  • Suárez-Santana, C.M., Sierra, E., Díaz-Delgado, J., Zucca, D., de Quirós, Y.B., Puig-Lozano, R., Câmara, N., De la Fuente, J., de Los Monteros, A.E., Rivero, M., et al. (2018). Prostatic lesions in Odontocete Cetaceans. Vet Pathol 55, 466–472.

    Article  PubMed  Google Scholar 

  • Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J., and Rambaut, A. (2018). Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4, vey016.

    Article  PubMed  PubMed Central  Google Scholar 

  • Swierstra, E.E. (1968). A comparison of spermatozoa production and spermatozoa output of yorkshire and lacombe boars. Reproduction 17, 459–469.

    Article  CAS  Google Scholar 

  • Tamura, K., Stecher, G., and Kumar, S. (2021). MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38, 3022–3027.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thirumalai, A., and Page, S.T. (2019). Recent developments in male contraception. Drugs 79, 11–20.

    Article  CAS  PubMed  Google Scholar 

  • Turner, T.T. (1995). On the epididymis and its role in the development of the fertile ejaculate. J Androl 16, 292–298.

    CAS  PubMed  Google Scholar 

  • van Der Horst, G., Seier, J.V., Spinks, A.C., and Hendricks, S. (1999). The maturation of sperm motility in the epididymis and vas deferens of the vervet monkey, Cercopithecus aethiops. Int J Androl 22, 197–207.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Hu, J., Song, L., Rong, E., Yang, C., Chen, X., Pu, J., Sun, H., Gao, C., Burt, D.W., et al. (2022). Functional divergence of oligoadenylate synthetase 1 (OAS1) proteins in Tetrapods. Sci China Life Sci 65, 1395–1412.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Z., Xu, S., Du, K., Huang, F., Chen, Z., Zhou, K., Ren, W., and Yang, G. (2016). Evolution of digestive enzymes and RNASE1 provides insights into dietary switch of cetaceans. Mol Biol Evol 33, 3144–3157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wertheim, J.O., Murrell, B., Smith, M.D., Kosakovsky Pond, S.L., and Scheffler, K. (2015). RELAX: detecting relaxed selection in a phylogenetic framework. Mol Biol Evol 32, 820–832.

    Article  CAS  PubMed  Google Scholar 

  • Westmuckett, A.D., Nguyen, E.B., Herlea-Pana, O.M., Alvau, A., Salicioni, A.M., and Moore, K.L. (2014). Impaired sperm maturation in Rnase9 knockout mice. Biol Reprod 90, 120.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wheeler, T.T., Maqbool, N.J., and Gupta, S.K. (2012). Mapping, phylogenetic and expression analysis of the RNase (RNaseA) locus in cattle. J Mol Evol 74, 237–248.

    Article  CAS  PubMed  Google Scholar 

  • Xu, H., Liu, Y., Meng, F., He, B., Han, N., Li, G., Rossiter, S.J., and Zhang, S. (2013). Multiple bursts of pancreatic ribonuclease gene duplication in insect-eating bats. Gene 526, 112–117.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z. (1998). Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15, 568–573.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z. (2000). Maximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A. J Mol Evol 51, 423–432.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z. (2005). The power of phylogenetic comparison in revealing protein function. Proc Natl Acad Sci USA 102, 3179–3180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24, 1586–1591.

    Article  CAS  PubMed  Google Scholar 

  • Yin, D., Zhou, R.R., Yin, M., Chen, Y., Xu, S., and Yang, G. (2021a). Gene duplication and loss of AANAT in mammals driven by rhythmic adaptations. Mol Biol Evol 38, 3925–3937.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin, Y., Fan, H., Zhou, B., Hu, Y., Fan, G., Wang, J., Zhou, F., Nie, W., Zhang, C., Liu, L., et al. (2021b). Molecular mechanisms and topological consequences of drastic chromosomal rearrangements of muntjac deer. Nat Commun 12, 6858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, L., and Zhang, Y. (2006). The unusual adaptive expansion of pancreatic ribonuclease gene in carnivora. Mol Biol Evol 23, 2326–2335.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J., Dyer, K.D., and Rosenberg, H.F. (2000). Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. Proc Natl Acad Sci USA 97, 4701–4706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., Nielsen, R., and Yang, Z. (2005). Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22, 2472–2479.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J., Zhang, Y., and Rosenberg, H.F. (2002). Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nat Genet 30, 411–415.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, H., Yang, J.R., Xu, H., and Zhang, J. (2010). Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo. Mol Biol Evol 27, 2669–2673.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, W., Ahmed, S., Ahmed, S., Yangliu, Y., Wang, H., and Cai, X. (2021). Analysis of long non-coding RNAs in epididymis of cattleyak associated with male infertility. Theriogenology 160, 61–71.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, X., Wang, B., Pan, Q., Zhang, J., Kumar, S., Sun, X., Liu, Z., Pan, H., Lin, Y., Liu, G., et al. (2014). Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history. Nat Genet 46, 1303–1310.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, X., Xu, S., Yang, Y., Zhou, K., and Yang, G. (2011). Phylogenomic analyses and improved resolution of Cetartiodactyla. Mol PhyloGenet Evol 61, 255–264.

    Article  PubMed  Google Scholar 

  • Zhu, C.F., Liu, Q., Zhang, L., Yuan, H.X., Zhen, W., Zhang, J.S., Chen, Z. J., Hall, S.H., French, F.S., and Zhang, Y.L. (2007). RNase9, an androgen-dependent member of the RNase A family, is specifically expressed in the rat epididymis. Biol Reprod 76, 63–73.

    Article  CAS  PubMed  Google Scholar 

  • Zurano, J.P., Magalhães, F.M., Asato, A.E., Silva, G., Bidau, C.J., Mesquita, D.O., and Costa, G.C. (2019). Cetartiodactyla: updating a time-calibrated molecular phylogeny. Mol Phylogenet Evol 133, 256–262.

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Special Basic Cooperative Research Programs of Yunnan Provincial Undergraduate Universities (202001AO070195), the National Natural Science Foundation of China (31925006), and the Applied Basic Research General Project of Yunnan Science Technology Department (202001BB050058).

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Authors and Affiliations

  1. School of Life Sciences, Yunnan University, Kunming, 650500, China

    Datian Lang, Xiaoping Wang, Chunbing Liu, Weihang Geng, Li Yu & Heng Xiao

  2. School of Ecology and Environmental Science, Yunnan University, Kunming, 650091, China

    Shanyuan Chen, Chunqing Li & Heng Xiao

  3. State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, 650091, China

    Xiaoping Wang, Chunbing Liu, Weihang Geng & Li Yu

  4. Biodiversity Research Center of Wumeng Mountain, Department of Agronomy and Life Science, Zhaotong University, Zhaotong, 657000, China

    Datian Lang

  5. Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, M5S 1A8, Canada

    David M. Irwin

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  1. Datian Lang
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Lang, D., Wang, X., Liu, C. et al. Birth-and-death evolution of ribonuclease 9 genes in Cetartiodactyla. Sci. China Life Sci. 66, 1170–1182 (2023). https://doi.org/10.1007/s11427-022-2195-x

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