Rapid adaptation to a novel pathogen through disease tolerance in a wild songbird

. 2023 Jun ; 19 (6) : e1011408. [epub] 20230609

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37294834
Odkazy

PubMed 37294834
PubMed Central PMC10287013
DOI 10.1371/journal.ppat.1011408
PII: PPATHOGENS-D-22-02115
Knihovny.cz E-zdroje

Animal hosts can adapt to emerging infectious disease through both disease resistance, which decreases pathogen numbers, and disease tolerance, which limits damage during infection without limiting pathogen replication. Both resistance and tolerance mechanisms can drive pathogen transmission dynamics. However, it is not well understood how quickly host tolerance evolves in response to novel pathogens or what physiological mechanisms underlie this defense. Using natural populations of house finches (Haemorhous mexicanus) across the temporal invasion gradient of a recently emerged bacterial pathogen (Mycoplasma gallisepticum), we find rapid evolution of tolerance (<25 years). In particular, populations with a longer history of MG endemism have less pathology but similar pathogen loads compared with populations with a shorter history of MG endemism. Further, gene expression data reveal that more-targeted immune responses early in infection are associated with tolerance. These results suggest an important role for tolerance in host adaptation to emerging infectious diseases, a phenomenon with broad implications for pathogen spread and evolution.

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Daszak P, Cunningham AA, Hyatt AD. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science. 2000;287(5452):443–9. doi: 10.1126/science.287.5452.443 PubMed DOI

VanderWaal K, Deen J. Global trends in infectious diseases of swine. Proceedings of the National Academy of Sciences. 2018;115(45):11495–500. doi: 10.1073/pnas.1806068115 PubMed DOI PMC

Fisher MC, Gurr SJ, Cuomo CA, Blehert DS, Jin H, Stukenbrock EH, et al.. Threats posed by the fungal kingdom to humans, wildlife, and agriculture. MBio. 2020;11(3):e00449–20. doi: 10.1128/mBio.00449-20 PubMed DOI PMC

Voyles J, Woodhams DC, Saenz V, Byrne AQ, Perez R, Rios-Sotelo G, et al.. Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science. 2018;359(6383):1517–9. doi: 10.1126/science.aao4806 PubMed DOI

Langwig KE, Hoyt JR, Parise KL, Frick WF, Foster JT, Kilpatrick AM. Resistance in persisting bat populations after white-nose syndrome invasion. Philosophical Transactions of the Royal Society B: Biological Sciences. 2017;372(1712): 20160044. PubMed PMC

Alves JM, Carneiro M, Cheng JY, Lemos de Matos A, Rahman MM, Loog L, et al.. Parallel adaptation of rabbit populations to myxoma virus. Science. 2019;363(6433):1319–26. doi: 10.1126/science.aau7285 PubMed DOI PMC

Råberg L. How to live with the enemy: understanding tolerance to parasites. PLoS Biology. 2014;12(11):e1001989. doi: 10.1371/journal.pbio.1001989 PubMed DOI PMC

Råberg L, Graham AL, Read AF. Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences. 2008;364(1513):37–49. PubMed PMC

Simms EL. Defining tolerance as a norm of reaction. Evolutionary Ecology. 2000;14(4):563–70.

Bonneaud C, Tardy L, Giraudeau M, Hill GE, McGraw KJ, Wilson AJ. Evolution of both host resistance and tolerance to an emerging bacterial pathogen. Evolution Letters. 2019;3(5):544–54.

Burgan SC, Gervasi SS, Johnson LR, Martin LB. How individual variation in host tolerance affects competence to transmit parasites. Physiological and Biochemical Zoology. 2019;92(1):49–57. doi: 10.1086/701169 PubMed DOI

Henschen AE, Adelman JS. What does tolerance mean for animal disease dynamics when pathology enhances transmission? Integrative and Comparative Biology. 2019;59(5):1220–30. doi: 10.1093/icb/icz065 PubMed DOI

Savage AE, Zamudio KR. Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations. Proceedings of the Royal Society B: Biological Sciences. 2016;283(1827):20153115. PubMed PMC

Atkinson CT, Saili KS, Utzurrum RB, Jarvi SI. Experimental evidence for evolved tolerance to avian malaria in a wild population of low elevation Hawai’i ’Amakihi (Hemignathus virens). Ecohealth. 2013;10(4):366–75. doi: 10.1007/s10393-013-0899-2 PubMed DOI

Weber JN, Steinel NC, Peng F, Shim KC, Lohman BK, Fuess LE, et al.. Evolutionary gain and loss of a pathological immune response to parasitism. Science. 2022;377(6611):1206–11. doi: 10.1126/science.abo3411 PubMed DOI PMC

Ley DH, Berkhoff JE, McLaren JM. Mycoplasma gallisepticum isolated from house finches (Carpodacus mexicanus) with conjunctivitis. Avian Diseases. 1996;40(2):480–3. PubMed

Luttrell MP, Stallknecht DE, Fischer JR, Sewell CT, Kleven SH. Natural Mycoplasma gallisepticum infection in a captive flock of house finches. Journal of Wildlife Diseases. 1998;34(2):289–96. doi: 10.7589/0090-3558-34.2.289 PubMed DOI

Faustino CR, Jennelle CS, Connolly V, Davis AK, Swarthout EC, Dhondt AA, et al.. Mycoplasma gallisepticum infection dynamics in a house finch population: seasonal variation in survival, encounter and transmission rate. Journal of Animal Ecology. 2004;73(4):651–69.

Hochachka WM, Dhondt AA, Dobson A, Hawley DM, Ley DH, Lovette IJ. Multiple host transfers, but only one successful lineage in a continent-spanning emergent pathogen. Proceedings of the Royal Society B-Biological Sciences. 2013;280(1766): 20131068. PubMed PMC

Staley M, Bonneaud C, McGraw KJ, Vleck CM, Hill GE. Detection of Mycoplasma gallisepticum in house finches (Haemorhous mexicanus) from Arizona. Avian diseases. 2017;62(1):14–7. PubMed

Dhondt AA, Tessaglia DL, Slothower RL. Epidemic mycoplasmal conjunctivitis in house finches from eastern North America. Journal of Wildlife Diseases. 1998;34(2):265–80. doi: 10.7589/0090-3558-34.2.265 PubMed DOI

Fischer JR, Stallknecht DE, Luttrell P, Dhondt AA, Converse KA. Mycoplasmal conjunctivitis in wild songbirds: the spread of a new contagious disease in a mobile host population. Emerging Infectious Diseases. 1997;3(1):69–72. doi: 10.3201/eid0301.970110 PubMed DOI PMC

Duckworth RA, Badyaev AV, Farmer KL, Hill GE, Roberts SR. First case of Mycoplasma gallisepticum infection in the western range of the house finch (Carpodacus mexicanus). The Auk. 2003;120(2):528–30.

Dhondt AA, Badyaev AV, Dobson AP, Hawley DM, Driscoll MJ, Hochachka WM, et al.. Dynamics of mycoplasmal conjunctivitis in the native and introduced range of the host. EcoHealth. 2006;3(2):95–102.

Badyaev AV, Belloni V, Hill GE. House Finch (Haemorhous mexicanus), version 1.0. In Birds of the World: Cornell Lab of Ornithology, Ithaca, NY, USA; 2020.

Ley DH, Sheaffer DS, Dhondt AA. Further western spread of Mycoplasma gallisepticum infection of house finches. Journal of Wildlife Diseases. 2006;42(2):429–31. doi: 10.7589/0090-3558-42.2.429 PubMed DOI

Ley DH, Hawley DM, Geary SJ, Dhondt AA. House Finch (Haemorhous mexicanus) Conjunctivitis, and Mycoplasma spp. Isolated from North American Wild Birds, 1994–2015. Journal of Wildlife Diseases. 2016;52(3):669–73. PubMed PMC

Hochachka WM, Dhondt AA. Density-dependent decline of host abundance resulting from a new infectious disease. Proceedings of the National Academy of Sciences. 2000;97(10):5303. doi: 10.1073/pnas.080551197 PubMed DOI PMC

Adelman JS, Mayer C, Hawley DM. Infection reduces anti-predator behaviors in house finches. Journal of Avian Biology. 2017;48(4):519–28. doi: 10.1111/jav.01058 PubMed DOI PMC

Hawley DM, Fleischer RC. Contrasting epidemic histories reveal pathogen-mediated balancing selection on Class II MHC diversity in a wild songbird. PLoS One. 2012;7(1): e30222. doi: 10.1371/journal.pone.0030222 PubMed DOI PMC

Adelman JS, Kirkpatrick L, Grodio JL, Hawley DM. House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of Mycoplasma gallisepticum infection. The American Naturalist. 2013;181(5):674–89. doi: 10.1086/670024 PubMed DOI

Bonneaud C, Giraudeau M, Tardy L, Staley M, Hill GE, McGraw KJ. Rapid antagonistic coevolution in an emerging pathogen and its vertebrate host. Current Biology. 2018;28(18):2978–83. e5. doi: 10.1016/j.cub.2018.07.003 PubMed DOI

Garland T Jr, Adolph SC. Why not to do two-species comparative studies: limitations on inferring adaptation. Physiological Zoology. 1994;67(4):797–828.

Glass EJ, Crutchley S, Jensen K. Living with the enemy or uninvited guests: Functional genomics approaches to investigating host resistance or tolerance traits to a protozoan parasite, Theileria annulata, in cattle. Veterinary Immunology and Immunopathology. 2012;148(1):178–89. doi: 10.1016/j.vetimm.2012.03.006 PubMed DOI PMC

Kamiya T, Davis NM, Greischar MA, Schneider D, Mideo N. Linking functional and molecular mechanisms of host resilience to malaria infection. Elife. 2021;10:e65846. doi: 10.7554/eLife.65846 PubMed DOI PMC

Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defense strategy. Science. 2012;335(6071):936–41. doi: 10.1126/science.1214935 PubMed DOI PMC

Sanchez KK, Chen GY, Schieber AMP, Redford SE, Shokhirev MN, Leblanc M, et al.. Cooperative metabolic adaptations in the host can favor asymptomatic infection and select for attenuated virulence in an enteric pathogen. Cell. 2018;175(1):146–58. e15. doi: 10.1016/j.cell.2018.07.016 PubMed DOI PMC

Prakash A, Monteith KM, Vale PF. Mechanisms of damage prevention, signalling and repair impact disease tolerance. Proceedings of the Royal Society B. 2022;289(1981):20220837. doi: 10.1098/rspb.2022.0837 PubMed DOI PMC

Becker DJ, Albery GF, Kessler MK, Lunn TJ, Falvo CA, Czirják GÁ, et al.. Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence. Journal of Animal Ecology. 2020;89(4):972–95. doi: 10.1111/1365-2656.13166 PubMed DOI PMC

Fleming-Davies AE, Williams PD, Dhondt AA, Dobson AP, Hochachka WM, Leon AE, et al.. Incomplete host immunity favors the evolution of virulence in an emergent pathogen. Science. 2018;359(6379):1030–3. doi: 10.1126/science.aao2140 PubMed DOI PMC

Nagy N, Oláh I, Vervelde L. Chapter 2—Structure of the avian lymphoid system. In: Kaspers B, Schat KA, Göbel TW, Vervelde L, editors. Avian Immunology (Third Edition). Boston: Academic Press; 2022. p. 11–44.

Pyle P. Molt limits in North American passerines. North American Bird Bander. 1997;22(2):49–89.

Hawley DM, Osnas EE, Dobson AP, Hochachka WM, Ley DH, Dhondt AA. Parallel patterns of increased virulence in a recently emerged wildlife pathogen. PLoS biology. 2013;11(5):e1001570. PubMed PMC

Hawley DM, Grodio J, Frasca S, Kirkpatrick L, Ley DH. Experimental infection of domestic canaries (Serinus canaria domestica) with Mycoplasma gallisepticum: a new model system for a wildlife disease. Avian Pathology. 2011;40(3):321–7. doi: 10.1080/03079457.2011.571660 PubMed DOI

Sydenstricker KV, Dhondt AA, Hawley DM, Jennelle CS, Kollias HW, Kollias GV. Characterization of experimental Mycoplasma gallisepticum infection in captive house finch flocks. Avian Diseases. 2006;50(1):39–44. doi: 10.1637/7403-062805R.1 PubMed DOI

Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Methods. 2012;9(7):671–5. doi: 10.1038/nmeth.2089 PubMed DOI PMC

Grodio JL, Dhondt KV, O’Connell PH, Schat KA. Detection and quantification of Mycoplasma gallisepticum genome load in conjunctival samples of experimentally infected house finches (Carpodacus mexicanus) using real-time polymerase chain reaction. Avian Pathology. 2008;37(4):385–91. doi: 10.1080/03079450802216629 PubMed DOI

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 PubMed DOI PMC

Sequence Read Archive (SRA) [Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information; 2009 - [cited 2023]. Available from: http://www.ncbi.nlm.nih.gov/bioproject/973136.

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al.. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology. 2011;29(7):644–52. doi: 10.1038/nbt.1883 PubMed DOI PMC

Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al.. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature protocols. 2013;8(8):1494–512. doi: 10.1038/nprot.2013.084 PubMed DOI PMC

Seppey M, Manni M, Zdobnov EM. BUSCO: Assessing Genome Assembly and Annotation Completeness. Methods in Molecular Biology. 2019;1962:227–45. doi: 10.1007/978-1-4939-9173-0_14 PubMed DOI

Bentz AB, Thomas GWC, Rusch DB, Rosvall KA. Tissue-specific expression profiles and positive selection analysis in the tree swallow (Tachycineta bicolor) using a de novo transcriptome assembly. Scientific Reports. 2019;9(1):15849. doi: 10.1038/s41598-019-52312-4 PubMed DOI PMC

Dolinski AC, Homola JJ, Jankowski MD, Owen JC. De novo transcriptome assembly and data for the blue-winged teal (Spatula discors). Data Brief. 2020;30:105380. doi: 10.1016/j.dib.2020.105380 PubMed DOI PMC

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature methods. 2012;9(4):357–9. doi: 10.1038/nmeth.1923 PubMed DOI PMC

Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC bioinformatics. 2011;12(1):1–16. PubMed PMC

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. doi: 10.1093/bioinformatics/btp616 PubMed DOI PMC

Bryant DM, Johnson K, DiTommaso T, Tickle T, Couger MB, Payzin-Dogru D, et al.. A tissue-mapped axolotl de novo transcriptome enables identification of limb regeneration factors. Cell Reports. 2017;18(3):762–76. doi: 10.1016/j.celrep.2016.12.063 PubMed DOI PMC

Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, et al.. g: Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic acids research. 2019;47(W1):W191–W8. doi: 10.1093/nar/gkz369 PubMed DOI PMC

Reimand J, Kull M, Peterson H, Hansen J, Vilo J. g: Profiler—a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic acids research. 2007;35(suppl_2):W193–W200. doi: 10.1093/nar/gkm226 PubMed DOI PMC

Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al.. Gene ontology: tool for the unification of biology. Nature genetics. 2000;25(1):25–9. PubMed PMC

The Gene Ontology resource: enriching a GOld mine. Nucleic acids research. 2021;49(D1):D325–D34. doi: 10.1093/nar/gkaa1113 PubMed DOI PMC

Kanehisa M. Toward understanding the origin and evolution of cellular organisms. Protein Science. 2019;28(11):1947–51. doi: 10.1002/pro.3715 PubMed DOI PMC

Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe M. KEGG: integrating viruses and cellular organisms. Nucleic Acids Res. 2021;49(D1):D545–D51. doi: 10.1093/nar/gkaa970 PubMed DOI PMC

Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27–30. doi: 10.1093/nar/28.1.27 PubMed DOI PMC

Gillespie M, Jassal B, Stephan R, Milacic M, Rothfels K, Senff-Ribeiro A, et al.. The reactome pathway knowledgebase 2022. Nucleic acids research. 2022;50(D1):D687–D92. doi: 10.1093/nar/gkab1028 PubMed DOI PMC

Martens M, Ammar A, Riutta A, Waagmeester A, Slenter DN, Hanspers K, et al.. WikiPathways: connecting communities. Nucleic Acids Research. 2021;49(D1):D613–D21. doi: 10.1093/nar/gkaa1024 PubMed DOI PMC

Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A, et al.. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Research. 2006;34(suppl_1):D108–D10. doi: 10.1093/nar/gkj143 PubMed DOI PMC

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. Journal of Statistical Software. 2015;67(1):1–48.

Kuznetsova A, Brockhoff PB, Christensen RH. lmerTest package: tests in linear mixed effects models. Journal of statistical software. 2017;82:1–26.

Fox J, Weisberg S. An R companion to applied regression: Sage publications; 2018.

Knowles JE, Frederick C. merTools: Tools for analyzing mixed effect regression models. R package version 0.5. 2. 2020.

R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.

Råberg L, Sim D, Read AF. Disentangling Genetic Variation for Resistance and Tolerance to Infectious Diseases in Animals. Science. 2007;318(5851):812. doi: 10.1126/science.1148526 PubMed DOI

Henschen A, Adelman J. (2023). Data for: Rapid adaptation to a novel pathogen through disease tolerance in a wild songbird. Dryad, Dataset, 10.5061/dryad.v9s4mw71r. PubMed DOI PMC

Becker R, Wilks A, Brownrigg R, Minka T, Deckmyn A. maps: Draw Geographical Maps. R package version 3.4.0. 2018. 2021.

Burnham KP, Anderson DR. A practical information-theoretic approach. Model selection and multimodel inference. 2002;2.

Lenth RV. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 155–1. 2021.

Holm S. A simple sequentially rejective multiple test procedure. Scandinavian journal of statistics. 1979:65–70.

Devleesschauwer B, Torgerson P, Charlier J, Levecke B, Praet N, Roelandt S, et al.. prevalence: Tools for prevalence assessment studies. R package version 0.4.1. 2022.

Bonneaud C, Balenger SL, Russell AF, Zhang J, Hill GE, Edwards SV. Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proceedings of the National Academy of Sciences. 2011;108(19):7866–71. PubMed PMC

Caum EL. The exotic birds of Hawaii: The Museum; 1933.

Elliott JJ, Arbib Jr RS. Origin and status of the house finch in the eastern United States. The Auk. 1953:31–7.

Bonneaud C, Tardy L, Hill GE, McGraw KJ, Wilson AJ, Giraudeau M. Experimental evidence for stabilizing selection on virulence in a bacterial pathogen. Evolution Letters. 2020;4(6):491–501. doi: 10.1002/evl3.203 PubMed DOI PMC

Ruden RM, Adelman JS. Disease tolerance alters host competence in a wild songbird. Biology Letters. 2021;17(10):20210362. PubMed PMC

Hawley DM, Thomason CA, Aberle MA, Brown R, Adelman JS. High virulence is associated with pathogen spreadability in a songbird–bacterial system. Royal Society Open Science. 2023;10(1):220975. doi: 10.1098/rsos.220975 PubMed DOI PMC

Wang Z, Farmer K, Hill GE, Edwards SV. A cDNA macroarray approach to parasite-induced gene expression changes in a songbird host: Genetic response of house finches to experimental infection by Mycoplasma gallisepticum. Molecular Ecology. 2006;15(5):1263–73. doi: 10.1111/j.1365-294X.2005.02753.x PubMed DOI

Bonneaud C, Balenger SL, Zhang J, Edwards SV, Hill GE. Innate immunity and the evolution of resistance to an emerging infectious disease in a wild bird. Molecular ecology. 2012;21(11):2628–39. doi: 10.1111/j.1365-294X.2012.05551.x PubMed DOI

Wang S, Song R, Wang Z, Jing Z, Wang S, Ma J. S100A8/A9 in Inflammation. Frontiers in immunology. 2018;9:1298. doi: 10.3389/fimmu.2018.01298 PubMed DOI PMC

Sack Jr GH. Serum amyloid A–a review. Molecular medicine. 2018;24(1):46. doi: 10.1186/s10020-018-0047-0 PubMed DOI PMC

Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine & growth factor reviews. 2003;14(5):409–26. PubMed

Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K. Essential involvement of interleukin-8 (IL-8) in acute inflammation. Journal of Leukocyte Biology. 1994;56(5):559–64. PubMed

Lu J, Chatterjee M, Schmid H, Beck S, Gawaz M. CXCL14 as an emerging immune and inflammatory modulator. Journal of Inflammation. 2016;13(1):1–8. doi: 10.1186/s12950-015-0109-9 PubMed DOI PMC

Mägert H-Jr, Ständker L, Kreutzmann P, Zucht H-D, Reinecke M, Sommerhoff CP, et al.. LEKTI, a novel 15-domain type of human serine proteinase inhibitor. Journal of Biological Chemistry. 1999;274(31):21499–502. doi: 10.1074/jbc.274.31.21499 PubMed DOI

Cheng S, Di Z, Hirman AR, Zheng H, Duo L, Zhai Q, et al.. MiR-375-3p alleviates the severity of inflammation through targeting YAP1/LEKTI pathway in HaCaT cells. Bioscience, Biotechnology, and Biochemistry. 2020;84(10):2005–13. doi: 10.1080/09168451.2020.1783196 PubMed DOI

Vinkler M, Leon AE, Kirkpatrick L, Dalloul RA, Hawley DM. Differing house finch cytokine expression responses to original and evolved isolates of Mycoplasma gallisepticum. Frontiers in Immunology. 2018;9:13. doi: 10.3389/fimmu.2018.00013 PubMed DOI PMC

Liu Y, Beyer A, Aebersold R. On the dependency of cellular protein levels on mRNA abundance. Cell. 2016;165(3):535–50. doi: 10.1016/j.cell.2016.03.014 PubMed DOI

Heck M, Neely BA. Proteomics in non-model organisms: a new analytical frontier. Journal of Proteome Research. 2020;19(9):3595–606. doi: 10.1021/acs.jproteome.0c00448 PubMed DOI PMC

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