Divergence history and hydrothermal vent adaptation of decapod crustaceans: A mitogenomic perspective
Autoři:
Shao’e Sun aff001; Zhongli Sha aff001; Yanrong Wang aff001
Působiště autorů:
Deep Sea Research Center, Institute of Oceanology, Chinese Academy of Science, Qingdao, China
aff001; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, China
aff002; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China
aff003; University of Chinese Academy of Sciences, Beijing, China
aff004
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224373
Souhrn
Decapod crustaceans, such as alvinocaridid shrimps, bythograeid crabs and galatheid squat lobsters are important fauna in the hydrothermal vents and have well adapted to hydrothermal vent environments. In this study, eighteen mitochondrial genomes (mitogenomes) of hydrothermal vent decapods were used to explore the evolutionary history and their adaptation to the hydrothermal vent habitats. BI and ML algorithms produced consistent phylogeny for Decapoda. The phylogenetic relationship revealed more evolved positions for all the hydrothermal vent groups, indicating they migrated from non-vent environments, instead of the remnants of ancient hydrothermal vent species, which support the extinction/repopulation hypothesis. The divergence time estimation on the Alvinocarididae, Bythograeidae and Galatheoidea nodes are located at 75.20, 56.44 and 47.41–50.43 Ma, respectively, which refers to the Late Cretaceous origin of alvinocaridid shrimps and the Early Tertiary origin of bythograeid crabs and galatheid squat lobsters. These origin stories are thought to associate with the global deep-water anoxic/dysoxic events. Total eleven positively selected sites were detected in the mitochondrial OXPHOS genes of three lineages of hydrothermal vent decapods, suggesting a link between hydrothermal vent adaption and OXPHOS molecular biology in decapods. This study adds to the understanding of the link between mitogenome evolution and ecological adaptation to hydrothermal vent habitats in decapods.
Klíčová slova:
Phylogenetics – Phylogenetic analysis – Mitochondria – Shrimp – Evolutionary adaptation – Crabs – Lobsters – Hydrothermal vents
Zdroje
1. Little CTS, Vrijenhoek RC. Are hydrothermal vent animals living fossils? Trends in Ecology and Evolution. 2003; 18: 582–588. https://doi.org/10.1016/j.tree.2003.08.009
2. Van Dover CL. The Ecology of Deep-Sea Hydrothermal Vents. Princeton University Press, Princeton (NJ). 2000.
3. Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC. Evolution and biogeography of deep-sea vent and seep invertebrates. Science. 2002; 295: 1253–1257. doi: 10.1126/science.1067361 11847331
4. Martin JW, Haney TA. Decapod crustaceans from hydrothermal vents and cold seeps: A review through 2005. Zoological Journal of the Linnean Society. 2005; 145: 445–522. https://doi.org/10.1111/j.1096-3642.2005.00178.x
5. Yang JS, Lu B, Chen DF, Yu YQ, Yang F, Nagasawa H, et al. When did decapods invade hydrothermal vents? Clues from the Western Pacific and Indian Oceans. Molecular Biology and Evolution. 2013; 30: 305–309. doi: 10.1093/molbev/mss224 23002089
6. Newman WA. The abyssal hydrothermal vent fauna, a glimpse of antiquity. Bulletin of the Biological Society of Washington. 1985; 6: 231–243.
7. Jacobs DK, Lindberg DR. Oxygen and evolutionary patterns in the sea: Onshore/offshore trends and recent recruitment of deep-sea faunas. Proceedings of the National Academy of Sciences. 1998; 95: 9396–9401. https://doi.org/10.1073/pnas.95.16.9396
8. Shank TM, Black MB, Halanych KM, Lutz RA, Vrijenhoek RC. Miocene radiation of deep-sea hydrothermal vent shrimp (Caridea: Bresiliidae): Evidence from mitochondrial cytochrome oxidase subunit I. Molecular Phylogenetics and Evolution. 1999; 13: 244–254. doi: 10.1006/mpev.1999.0642 10603254
9. Sun SE, Sha ZL, Wang YR. Phylogenetic position of Alvinocarididae (Crustacea: Decapoda: Caridea): New insights into the origin and evolutionary history of the hydrothermal vent alvinocarid shrimps. Deep Sea Research Part I: Oceanographic Research Papers. 2018a; 141: 93–105. https://doi.org/10.1016/j.dsr.2018.10.001
10. Cheng R, Xue D, Galsworthy A, Han H. Complete mitochondrial genomes throw light on budding speciation in three Biston species (Lepidoptera, Geometridae). Zoologica Scripta. 2016; 46: 73–84. https://doi.org/10.1111/zsc.12184
11. Schuster A, Vargas S, Knapp IS, Pomponi SA, Toonen RJ, Erpenbeck D, et al. Divergence times in demosponges (Porifera): first insights from new mitogenomes and the inclusion of fossils in a birth-death clock model. BMC Evolutionary Biology. 2018; 18: 114. doi: 10.1186/s12862-018-1230-1 30021516
12. Yuan ML, Zhang QL, Zhang L, Jia CL, Li XP, Yang XZ, et al. Mitochondrial phylogeny, divergence history and high-altitude adaptation of grassland caterpillars (Lepidoptera: Lymantriinae: Gynaephora) inhabiting the Tibetan Plateau. Molecular Phylogenetics and Evolution. 2018; 122: 116–124. doi: 10.1016/j.ympev.2018.01.016 29408286
13. Inoue JG, Miya M, Lam K, Tay B-H, Danks JA, Bell J, et al. 2010. Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Molecular Biology and Evolution. 2010; 27: 2576–2586. doi: 10.1093/molbev/msq147 20551041
14. Pacheco MA, Battistuzzi FU, Lentino M, Aguilar RF, Kumar S, Escalante AA. Evolution of modern birds revealed by mitogenomics: timing the radiation and origin of major orders. Molecular Biology and Evolution. 2011; 28: 1927–1942. doi: 10.1093/molbev/msr014 21242529
15. San Mauro D, Gower DJ, Müller H, Loader SP, Zardoya R, Nussbaum RA, et al. Life-history evolution and mitogenomic phylogeny of caecilian amphibians. Molecular Phylogenetics and Evolution. 2014; 73: 177–189. doi: 10.1016/j.ympev.2014.01.009 24480323
16. Pozzi L, Hodgson JA, Burrell AS, Sterner KN, Raaum RL, Disotell TR. Primate phylogenetic relationships and divergence dates inferred from complete mitochondrial genomes. Molecular Phylogenetics and Evolution. 2014; 75: 165–183. doi: 10.1016/j.ympev.2014.02.023 24583291
17. Mohandesan E, Fitak RR, Corander J, Yadamsuren A, Chuluunbat B, Abdelhadi O, et al. Mitogenome sequencing in the genus Camelus reveals evidence for purifying selection and long-term divergence between wild and domestic bactrian camels. Scientific Reports. 2017; 7: 9970. doi: 10.1038/s41598-017-08995-8 28855525
18. Lin FJ, Liu Y, Sha Z, Tsang LM, Chu KH, Chan TY, et al. Evolution and phylogeny of the mud shrimps (Crustacea: Decapoda) revealed from complete mitochondrial genomes. BMC Genomics. 2012; 13: 631. doi: 10.1186/1471-2164-13-631 23153176
19. Pons J, Bauzà-Ribot MM, Jaume D, Juan C. Next-generation sequencing, phylogenetic signal and comparative mitogenomic analyses in Metacrangonyctidae (Amphipoda: Crustacea). BMC Genomics. 2014; 15: 566. doi: 10.1186/1471-2164-15-566 24997985
20. Sun SE, Sha ZL, Wang YR. Complete mitochondrial genome of the first deep-sea spongicolid shrimp Spongiocaris panglao (Decapoda: Stenopodidea): Novel gene arrangement and the phylogenetic position and origin of stenopodidea. Gene. 2018b; 676: 123–138. https://doi.org/10.1016/j.gene.2018.07.026
21. Das J. The role of mitochondrial respiration in physiological and evolutionary adaptation. Bioessays. 2006; 28: 890–901. doi: 10.1002/bies.20463 16937356
22. Shen YY, Liang L, Zhu ZH, Zhoua WP, Irwine DM, Zhang YP. Adaptive evolution of energy metabolism genes and the origin of flight in bats. Proceedings of the National Academy of Sciences. 2010; 107: 8666–8671. https://doi.org/10.1073/pnas.0912613107
23. Yang YX, Xu SX, Xu JX, Guo Y, Yang G. Adaptive evolution of mitochondrial energy metabolism genes associated with increased energy demand in flying insects. PLoS ONE. 2014; 9: e99120. doi: 10.1371/journal.pone.0099120 24918926
24. Garvin MR, Bielawski JP, Gharrett AJ. Positive Darwinian selection in the piston that powers proton pumps in Complex I of the mitochondria of Pacific salmon. PLoS ONE. 2011; 6: e24127. doi: 10.1371/journal.pone.0024127 21969854
25. da Fonseca RR, Johnson WE, O'Brien SJ, Ramos MJ, Antunes A. The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics. 2008; 9: 119. doi: 10.1186/1471-2164-9-119 18318906
26. Garvin MR, Thorgaard GH, Narum SR. Differential expression of genes that control respiration contribute to thermal adaptation in redband trout (Oncorhynchus mykiss gairdneri). Genome Biology and Evolution. 2015a; 7: 1404–1414. https://doi.org/10.1093/gbe/evv078
27. Sun SE, Li Q, Kong LF, Yu H. Limited locomotive ability relaxed selective constraints on molluscs mitochondrial genomes. Scientific Reports. 2017; 7: 10628. doi: 10.1038/s41598-017-11117-z 28878314
28. Zhang F, Broughton RE. Heterogeneous natural selection on oxidative phosphorylation genes among fishes with extreme high and low aerobic performance. BMC Evolutionary Biology. 2015; 15: 173. doi: 10.1186/s12862-015-0453-7 26306407
29. Welch AJ, Bedoya-Reina OC, Carretero-Paulet L, Miller W, Rode KD, Lindqvist C. Polar bears exhibit genome-wide signatures of bioenergetic adaptation to life in the arctic environment. Genome Biology and Evolution. 2014; 6: 433–450. doi: 10.1093/gbe/evu025 24504087
30. Bettencourt R, Pinheiro M, Egas C, Gomes P, Afonso M, Shank T, et al. High-throughput sequencing and analysis of the gill tissue transcriptome from the deep-sea hydrothermal vent mussel Bathymodiolus azoricus. BMC Genomics. 2010; 11: 559. doi: 10.1186/1471-2164-11-559 20937131
31. Thomas H, Claire B, Judith E, Nadine R. Deep transcriptome-sequencing and proteome analysis of the hydrothermal vent annelid Alvinella pompejana identifies the CvP-bias as a robust measure of eukaryotic thermostability. Biology Direct. 2013; 8: 2. doi: 10.1186/1745-6150-8-2 23324115
32. Cottin D, Shillito B, Chertemps T, Tanguy A, Léger N, Ravaux J. Identification of differentially expressed genes in the hydrothermal vent shrimp Rimicaris exoculata exposed to heat stress. Marine Genomics. 2010; 3: 71–78. doi: 10.1016/j.margen.2010.05.002 21798199
33. Zhang J, Sun QL, Luan ZD, Lian C, Sun L. Comparative transcriptome analysis of Rimicaris sp. reveals novel molecular features associated with survival in deep-sea hydrothermal vent. Scientific Reports. 2017a; 7: 2000. https://doi.org/10.1038/s41598-017-02073-9
34. Hui M, Cheng J, Sha Z. Adaptation to the deep-sea hydrothermal vents and cold seeps: Insights from the transcriptomes of Alvinocaris longirostris, in both environments. Deep Sea Research Part I: Oceanographic Research Papers. 2018; 135: 23–33. https://doi.org/10.1016/j.dsr.2018.03.014
35. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology. 2008; 57: 758–771. doi: 10.1080/10635150802429642 18853362
36. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003; 19: 1572–1574. doi: 10.1093/bioinformatics/btg180 12912839
37. Drummond AJ. Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology. 2007; 7: 214. doi: 10.1186/1471-2148-7-214 17996036
38. Posada D. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution. 2008; 25: 1253–1256. doi: 10.1093/molbev/msn083 18397919
39. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution. 2012; 29: 1969–1973. doi: 10.1093/molbev/mss075 22367748
40. Rambaut A. FigTree v1.4.0: Tree Figure Drawing Tool. Available from: http://tree.bio.ed.ac.uk/software/figtree. 2012.
41. Bracken HD, Grave SD, Toon A, Felder DL, Crandall KA. Phylogenetic position, systematic status, and divergence time of the Procarididea (Crustacea: Decapoda). Zoologica Scripta. 2010; 39: 198–212. https://doi.org/10.1111/j.1463-6409.2009.00410.x
42. Garassino A, Bravi S. Palaemon antonellae new species (Crustacea, Decapoda, Caridea) from the lower cretaceous ‘Platydolomite’ of Profeti (Caserta, Italy). Journal of Paleontology. 2003; 77: 589–592. https://doi.org/10.1017/S0022336000044279
43. Rabadà D. Crustáceos decápodos lacustres de las calizas litográficas del Cretácico inferior de España: las Hoyas (Cuenca) y el Montsec de Rúbies (Lleida). Cuadernos de Geología Ibérica. 1993; 17: 345–370.
44. Chablais J, Feldmann RM, Schweitzer CE. A new Triassic decapod, Platykotta akaina, from the Arabian shelf of the northern United Arab Emirates: earliest occurrence of the Anomura. Paläontologische Zeitschrift. 2011; 85: 93–102. https://doi.org/10.1007/s12542-010-0080-y
45. Amati L, Feldmann R, Zonneveld J. A new family of Triassic lobsters (Decapoda: Astacidea) from British Columbia and its phylogenetic context. Journal of Paleontology. 2004; 78: 150–168. https://doi.org/10.1666/0022-3360(2004)078<0150:ANFOTL>2.0.CO;2
46. Yang Z. PAML4: a program package for phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution. 2007; 24: 1586–1591. doi: 10.1093/molbev/msm088 17483113
47. Yang Z, Nielsen R, Goldman N, Pedersen AM. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics, 2000; 155: 431–449. https://doi.org/10.1002/1526-968X(200005)27:1<32::AID-GENE50>3.0.CO;2-T 10790415
48. Gillespie JH. The Causes of Molecular Evolution. Oxford University Press, Oxford. 1991.
49. Zhang J, Nielsen R, Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology and Evolution. 2005; 22: 2472–2479. doi: 10.1093/molbev/msi237 16107592
50. Yang Z, Wong WS, Nielsen R. Bayes empirical Bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution. 2005; 22: 1107–1118. doi: 10.1093/molbev/msi097 15689528
51. Cameron SL. Insect mitochondrial genomics: implications for evolution and phylogeny. Annual Review of Entomology. 2014; 59: 95–117. doi: 10.1146/annurev-ento-011613-162007 24160435
52. Mao M, Gibson T, Dowton M. Higher-level phylogeny of the Hymenoptera inferred from mitochondrial genomes. Molecular Phylogenetics and Evolution. 2015; 84: 34–43. doi: 10.1016/j.ympev.2014.12.009 25542648
53. Yuan ML, Zhang QL, Zhang L, Guo ZL, Liu YJ, Shen YY, et al. High-level phylogeny of the Coleoptera inferred with mitochondrial genome sequences. Molecular Phylogenetics and Evolution. 2016; 104: 99–111. doi: 10.1016/j.ympev.2016.08.002 27497607
54. Clarke CR, Karl SA, Horn RL, Bernard AM, Lea JS, Hazin FH, et al. Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis. Marine Biology. 2015; 162: 945–955. https://doi.org/10.1007/s00227-015-2636-6
55. Hsu KC, Bor H, Lin HD, Kuo PH, Tan MS, Chiu YW. Mitochondrial DNA phylogeography of Semisulcospira libertina (Gastropoda: Cerithioidea: Pleuroceridae): implications the history of landform changes in Taiwan. Molecular Biology Reports. 2014; 41: 3733–3743. doi: 10.1007/s11033-014-3238-y 24584517
56. Osigus H-J, Eitel M, Bernt M, Donath A, Schierwater B. Mitogenomics at the base of Metazoa. Molecular Phylogenetics and Evolution. 2013; 69: 339–351. doi: 10.1016/j.ympev.2013.07.016 23891951
57. Pavlova A, Gan HM, Lee YP, Austin CM, Gilligan DM, Lintermans M, et al. Purifying selection and genetic drift shaped Pleistocene evolution of the mitochondrial genome in an endangered Australian freshwater fish. Heredity. 2017; 118: 466–476. doi: 10.1038/hdy.2016.120 28051058
58. Harnik PG, Lotze HK, Anderson SC, Finkel ZV, Finnegan S, Lindberg DR, et al. Extinctions in ancient andmodern seas. Trends Ecology and Evolution. 2012; 27: 608–617. doi: 10.1016/j.tree.2012.07.010 22889500
59. Rogers AD. The role of the oceanic oxygen minima in generating biodiversity in the deep sea. Deep Sea Research Part II: Topical Studies in Oceanography. 2000; 47: 119–148. https://doi.org/10.1016/S0967-0645(99)00107-1
60. Castellana S, Vicario S, Saccone C. Evolutionary patterns of the mitochondrial genome in Metazoa: Exploring the role of mutation and selection in mitochondrial protein-coding genes. Genome Biology and Evolution. 2011; 3: 1067–1079. doi: 10.1093/gbe/evr040 21551352
61. Martin AP, Palumbi SR. Body size, metabolic rate, generation time, and the molecular clock. Proceedings of the National Academy of Sciences. 1993; 90: 4087–4091. https://doi.org/10.2307/2361897
62. Garvin MR, Bielwaski JP, Sazanov LA, Gharrett AJ. Review and meta-analysis of natural selection in mitochondrial Complex I in metazoans. Journal of Zoological Systematics and Evolutionary Research. 2015b; 53: 1–17. https://doi.org/10.1111/jzs.12079
63. Ballard J, Whitlock M. The incomplete natural history of mitochondria. Molecular Ecology. 2004; 13: 729–744. doi: 10.1046/j.1365-294x.2003.02063.x 15012752
64. Sazanov LA, Baradaran R, Efremov RG, Berrisford JM, Minhas G. A long road towards the structure of respiratory complex I, a giant molecular proton pump. Biochemical Society Transactions. 2013; 41: 1265–1271. doi: 10.1042/BST20130193 24059518
65. Zhang B, Zhang YH, Wang X, Zhang HX, Lin Q. The mitochondrial genome of a sea anemone Bolocera sp. exhibits novel genetic structures potentially involved in adaptation to the deep-sea environment. Ecology and Evolution. 2017b; 7: 4951–4962. doi: 10.1002/ece3.3067 28690821
66. Wang Z, Shi X, Sun L, Bai Y, Zhang D, Tang B. Evolution of mitochondrial energy metabolism genes associated with hydrothermal vent adaption of alvinocaridid shrimps. Genes and Genomics. 2017; 39: 1367–1376. https://doi.org/10.1007/s13258-017-0600-1
67. Xu S, Luosang J, Hua S, He J, Ciren A, Wang W, et al. High altitude adaptation and phylogenetic analysis of Tibetan horse based on the mitochondrial genome. Journal of Genetics and Genomics, 2007; 34: 720–729. doi: 10.1016/S1673-8527(07)60081-2 17707216
68. Ning T, Xiao H, Li J, Hua S, Zhang YP. Adaptive evolution of the mitochondrial NADH6 gene in the domestic horse. Genetics and Molecular Research. 2010; 9: 144–150. doi: 10.4238/vol9-1gmr705 20198570
69. Yu L, Wang X, Ting N, Zhang Y. Mitogenomic analysis of Chinese snub-nosed monkeys: Evidence of positive selection in NADH dehydrogenase genes in high-altitude adaptation. Mitochondrion, 2011; 11: 497–503. doi: 10.1016/j.mito.2011.01.004 21292038
70. Zhou T, Shen X, Irwin DM, Shen Y, Zhang Y. Mitogenomic analyses propose positive selection in mitochondrial genes for high-altitude adaptation in galliform birds. Mitochondrion. 2014; 18: 70–75. doi: 10.1016/j.mito.2014.07.012 25110061
71. Hassanin A, Ropiquet A, Couloux A, Cruaud C. Evolution of the mitochondrial genome in mammals living at high altitude: new insights from a study of the tribe caprini (Bovidae, Antilopinae). Journal of Molecular Evolution. 2009; 68; 293–310. doi: 10.1007/s00239-009-9208-7 19294454
72. Sazanov LA. A giant molecular proton pump: structure and mechanism of respiratory complex I. Nature Reviews Molecular Cell Biology. 2015; 16: 375–388. doi: 10.1038/nrm3997 25991374
73. Xu S, Yang YZ, Zhou J, Jing GE, Chen YT, Wang J, et al. A mitochondrial genome sequence of the Tibetan antelope (Pantholops hodgsonii). Genomics, Proteomics and Bioinformatics. 2005; 3: 5–17. doi: 10.1016/S1672-0229(05)03003-2 16144518
74. Luo Y, Gao W, Gao Y, Tang S, Huang Q, Tan X, et al. Mitochondrial genome analysis of Ochotona curzoniae and implication of cytochrome c oxidase in hypoxic adaptation. Mitochondrion. 2008; 8: 352–357. doi: 10.1016/j.mito.2008.07.005 18722554
75. Di Rocco F, Parisi G, Zambelli A, Vida-Rioja L. Rapid evolution of cytochrome c oxidase subunit II in camelids (Tylopoda, Camelidae). Journal of Bioenergetics and Biomembranes. 2006; 38: 293–297. doi: 10.1007/s10863-006-9048-8 17151935
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis