Abstract
Pathogen diversity is a key source of selective pressure on immune system genes, shaping molecular evolution mainly on widely distributed or migratory organisms such as cetaceans. Here, we investigated the effects of latitudinal span migration, different biomes occupation, and pathogen-mediated selection on MHC DQB locus divergence on cetaceans. We applied some evolutionary genetics methods using a dataset of 15 species and 121 sequences, and we found a trend on greater MHC divergence on tropical species when compared with either temperate or migratory species. In addition, oceanic cetaceans exhibit greater MHC divergence. Here, we show that, despite there was a correlation between the diversity of MHC DQB alleles with the distribution of organisms, the pattern of diversity found is not completely explained by pathogenic pressure, suggesting that other factors must be investigated for a better understanding of the processes related to the diversity of MHC in cetaceans.
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Baker CS, Vant MD, Dalebout ML, Lento GM, O’Brien SJ, Yuhki N (2006) Diversity and duplication of DQB and DRB-like genes of the MHC in baleen whales (suborder: Mysticeti). Immunogenetics 58:283–296. https://doi.org/10.1007/s00251-006-0080-y
Bordes F, Guégan JF, Morand S (2011) Microparasite species richness in rodents is higher at lower latitudes and is associated with reduced litter size. Oikos 120:1889–1896. https://doi.org/10.1111/j.1600-0706.2011.19314.x
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Cortazar-Chinarro M, Meyer-Lucht Y, Laurila A, Höglund J (2018) Signatures of historical selection on MHC reveal different selection patterns in the moor frog (Rana arvalis). Immunogenetics 70:477–484. https://doi.org/10.1007/s00251-017-1051-1
Díez-Rivero CM, Reche P (2009) Discovery of Conserved Epitopes Through Sequence Variability Analyses. In: Discovery of conserved epitopes through sequence variability analyses. Bioinformatics for Immunomics, vol 3. Springer, New York, pp 95–101. https://doi.org/10.1007/978-1-4419-0540-6_8
Drake GJ, Kennedy LJ, Auty HK et al (2004) The use of reference strand-mediated conformational analysis for the study of cheetah (Acinonyx jubatus) feline leucocyte antigen class II DRB polymorphisms. Mol Ecol 13:221–229. https://doi.org/10.1046/j.1365-294x.2003.02027.x
Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311. https://doi.org/10.1016/S0169-5347(98)01416-5
Garcia-Boronat M, Diez-Rivero CM, Reinherz EL, Reche PA (2008) PVS: a web server for protein sequence variability analysis tuned to facilitate conserved epitope discovery. Nucleic Acid Res 36:W35–W41. https://doi.org/10.1093/nar/gkn211
Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227. https://doi.org/10.1038/35012228
Guernier V, Hochberg ME, Guégan J-F (2004) Ecology drives the worldwide distribution of human diseases. PLoS Biol 2:e141. https://doi.org/10.1371/journal.pbio.0020141
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Soft 33:1–22. https://doi.org/10.18637/jss.v033.i02
IUCN/CSG (2019) IUCN – SSC Cetacean Specialist Group. https://iucn-csg.org. Accessed 3 Oct 2019
Jefferson TA, Webber MA, Pitman RL (2015) Marine mammals of the world: a comprehensive guide to their identification. Elsevier Science
Kassambara A (2018) Ggpubr: “ggplot2” based publication ready plots
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162. https://doi.org/10.1016/0198-8859(87)90066-8
Kriener K, O’hUigin C, Tichy H, Klein J (2000) Convergent evolution of major histocompatibility complex molecules in humans and New World monkeys. Immunogenetics 51:169–178. https://doi.org/10.1007/s002510050028
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lemoine F, Domelevo Entfellner J-B, Wilkinson E, Correia D, Dávila Felipe M, de Oliveira T, Gascuel O (2018) Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556:452–456. https://doi.org/10.1038/s41586-018-0043-0
Lenz TL, Eizaguirre C, Kalbe M, Milinski M (2013) Evaluating patterns of convergent evolution and trans-species polymorphism at MHC immunogenes in two sympatric stickleback species. Evolution 67:2400–2412. https://doi.org/10.1111/evo.12124
Mayer WE, Jonker M, Klein D, Ivanyi P, van Seventer G, Klein J (1988) Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution. EMBO J 7:2765–2774. https://doi.org/10.1002/j.1460-2075.1988.tb03131.x
Miller MA, Miller WA, Conrad PA, James ER, Melli AC, Leutenegger CM, Dabritz HA, Packham AE, Paradies D, Harris M, Ames J, Jessup DA, Worcester K, Grigg ME (2008) Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. Int J Parasitol 38:1319–1328. https://doi.org/10.1016/j.ijpara.2008.02.005
Miller MA, Byrne BA, Jang SS, Dodd EM, Dorfmeier E, Harris MD, Ames J, Paradies D, Worcester K, Jessup DA, Miller WA (2010) Enteric bacterial pathogen detection in southern sea otters (Enhydra lutris nereis) is associated with coastal urbanization and freshwater runoff. Vet Res 41:1. https://doi.org/10.1051/vetres/2009049
Møller AP (1998) Evidence of larger impact of parasites on hosts in the tropics: investment in immune function within and outside the tropics. Oikos 82:265. https://doi.org/10.2307/3546966
Moreno-Santillan DD, Lacey EA, Gendron D, Ortega J (2016) Genetic variation at exon 2 of the MHC class II DQB locus in blue whale (Balaenoptera musculus) from the Gulf of California. PLoS One 11:e0141296. https://doi.org/10.1371/journal.pone.0141296
Murray BW, Malik S, White BN (1995) Sequence variation at the major histocompatibility complex locus DQ beta in beluga whales (Delphinapterus leucas). Mol Biol Evol 12:582–593. https://doi.org/10.1093/oxfordjournals.molbev.a040238
Myers PRE, Parr CS, Jones T et al (2019) The Animal Diversity Web. https://animaldiversity.org. Accessed 3 Oct 2019
NCBI Resource Coordinators (2016) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 44(D1):D7–D19. https://doi.org/10.1093/nar/gkv1290
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Nigenda-Morales S, Flores-Ramirez S, Urban RJ, Vazquez-Juarez R (2008) MHC DQB-1 polymorphism in the Gulf of California fin whale (Balaenoptera physalus) population. J Hered 99:14–21. https://doi.org/10.1093/jhered/esm087
O’Connor EA, Cornwallis CK, Hasselquist D, Nilsson JÅ, Westerdahl H (2018) The evolution of immunity in relation to colonization and migration. Nat Ecol Evol 2:841–849. https://doi.org/10.1038/s41559-018-0509-3
Perrin WF (ed) (2009) Encyclopedia of marine mammals, 2nd edn. Academic Press, Burlington
R Core Team (2019) R: A language and environment for statistical computing
Robar N, Burness G, Murray DL (2010) Tropics, trophics and taxonomy: the determinants of parasite-associated host mortality. Oikos 119:1273–1280. https://doi.org/10.1111/j.1600-0706.2009.18292.x
Rohde K (2002) Ecology and biogeography of marine parasites. In: Advances in Marine Biology. Elsevier
Sayers EW, Agarwala R, Bolton EE, Brister JR, Canese K, Clark K, Connor R, Fiorini N, Funk K, Hefferon T, Holmes JB, Kim S, Kimchi A, Kitts PA, Lathrop S, Lu Z, Madden TL, Marchler-Bauer A, Phan L, Schneider VA, Schoch CL, Pruitt KD, Ostell J (2019) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 47:D23–D28. https://doi.org/10.1093/nar/gky1069
Stearns SC, Koella JC (eds) (2008) Evolution in health and disease, 2nd edn. Oxford University Press, Oxford
Trowsdale J, Groves V, Arnason A (1989) Limited MHC polymorphism in whales. Immunogenetics 29:19–24. https://doi.org/10.1007/BF02341609
van Bressem M, Raga A, Di Guardo G et al (2009) Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis Aquat Org 86:143–157. https://doi.org/10.3354/dao02101
Villanueva-Noriega MJ, Baker CS, Medrano-González L (2013) Evolution of the MHC-DQB exon 2 in marine and terrestrial mammals. Immunogenetics 65:47–61. https://doi.org/10.1007/s00251-012-0647-8
Wan Q-H, Zhu L, Wu H, Fang S-G (2006) Major histocompatibility complex class II variation in the giant panda (Ailuropoda melanoleuca). Mol Ecol 15:2441–2450. https://doi.org/10.1111/j.1365-294X.2006.02966.x
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer
Xu S, Chen B, Zhou K, Yang G (2008) High similarity at three MHC loci between the baiji and finless porpoise: trans-species or convergent evolution? Mol Phylogenet Evol 47:36–44. https://doi.org/10.1016/j.ympev.2007.05.026
Xu SX, Ren WH, Li SZ, Wei FW, Zhou KY, Yang G (2009) Sequence polymorphism and evolution of three cetacean MHC genes. J Mol Evol 69:260–275. https://doi.org/10.1007/s00239-009-9272-z
Yeager M, Hughes AL (1999) Evolution of the mammalian MHC: natural selection, recombination, and convergent evolution. Immunol Rev 167:45–58. https://doi.org/10.1111/j.1600-065X.1999.tb01381.x
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This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 and by FAPESP (2015/18269-1).
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Andreani, M.L., Freitas, L., Ramos, E.K.S. et al. Latitudinal diversity gradient and cetaceans from the perspective of MHC genes. Immunogenetics 72, 393–398 (2020). https://doi.org/10.1007/s00251-020-01171-9
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DOI: https://doi.org/10.1007/s00251-020-01171-9