Phylogenetic revision of Gymnotidae (Teleostei: Gymnotiformes), with descriptions of six subgenera

English version

Autoři: Jack M. Craig ^aff001; Lesley Y. Kim ^aff001; Victor A. Tagliacollo ^aff002; James S. Albert ^aff001
Působiště autorů: Department of Biology, University of Louisiana at Lafayette, Lafayette, LA, United States of America ^aff001; Museu de Zoologia da Universidade de São Paulo, São Paulo, São Paulo, Brazil ^aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224599

Souhrn

The diversity of gymnotid electric fishes has been intensely studied over the past 25 years, with 35 species named since 1994, compared to 11 species in the previous 236 years. Substantial effort has also been applied in recent years to documenting gymnotid interrelationships, with seven systematic studies published using morphological and molecular datasets. Nevertheless, until now, all gymnotids have been assigned to one of just two supraspecific taxa, the subfamily Electrophorinae with one genus Electrophorus and three valid species and the subfamily Gymnotine also with one genus Gymnotus and 43 valid species. This simple classification has obscured the substantial phenotypic and lineage diversity within the subfamily Gymnotine and hampered ecological and evolutionary studies of gymnotid biology. Here we present the most well-resolved and taxon-complete phylogeny of the Gymnotidae to date, including materials from all but one of the valid species. This phylogeny was constructed using a five-gene molecular dataset and a 115-character morphological dataset, enabling the inclusion of several species for which molecular data are still lacking. This phylogeny was time-calibrated using biogeographical priors in the absence of a fossil record. The tree topology is similar to those of previous studies, recovering all the major clades previously recognized with informal names. We propose a new gymnotid classification including two subfamilies (Electrophorinae and Gymnotinae) and six subgenera within the genus Gymnotus. Each subgenus exhibits a distinctive biogeographic distribution, within which most species have allopatric distributions and the subgenera are diverged from one another by an estimated 5–35 million years. We further provide robust taxonomic diagnoses, descriptions and identification keys to all gymnotid subgenera and all but four species. This new taxonomy more equitably partitions species diversity among supra-specific taxa, employing the previously vacant subgenus and subfamily ranks. This new taxonomy renders known gymnotid diversity more accessible to study by highlighting the deep divergences (chronological, geographical, genetic and morphological) among its several clades.

Klíčová slova:

Teeth – Jaw – Body limbs – Eyes – Mouth – Vertebrae – Maxilla – Chin

Zdroje

1. Craig JM, Crampton WGR, Albert JS. Revision of the polytypic electric fish Gymnotus carapo (Gymnotiformes, Teleostei), with descriptions of seven subspecies. Zootaxa. 2017;4318: 401–438.

2. Craig JM, Malabarba LR, Crampton WGR, Albert JS. Revision of Banded Knifefishes of the Gymnotus carapo and G. tigre clades (Gymnotidae Gymnotiformes) from the Southern Neotropics. Zootaxa. 2018;4379: 47–73. doi: 10.11646/zootaxa.4379.1.3 29689973

3. Albert JS, Crampton WGR. The Geography and Ecology of Diversification in Neotropical Freshwaters. Nat Knowl. 2010;1: 1–6. Available: http://www.nature.com/scitable/knowledge/library/the-geography-and-ecology-of-diversification-in-15667887

4. Crampton WGR. An Ecological Perspective on Diversity and Distributions. In: Albert JS, Reis RE dos, editors. Historical Biogeography of Neotropical Freshwater Fishes. 2011. pp. 165–189.

5. Albert JS, Crampton WGR. Seven new species of the Neotropical electric fish Gymnotus (Teleostei, Gymnotiformes) with a redescription of G. carapo (Linnaeus). Zootaxa. 2003;287: 1–54.

6. Albert JS, Crampton WGR. Five new species of Gymnotus (Teleostei: Gymnotiformes) from an upper Amazon floodplain, with descriptions of electric organ discharges and ecology. Ichthyol Explor Freshwat. 2001;12: 241–266.

7. Crampton WGR, Thorsen DH, Albert JS. Three New Species from a Diverse, Sympatric Assemblage of the Electric Fish Gymnotus (Gymnotiformes: Gymnotidae) in the Lowland Amazon Basin, with Notes on Ecology. Copeia. 2005. pp. 82–99. doi: 10.1643/CI-03-242R2

8. Albert JS, Miller RR. Gymnotus maculosus, a new species of electric fish (Chordata: Teleostei: Gymnotoidei) from Middle America, with a key to species of Gymnotus. Proc Biol Soc Washingt. 1995;108: 662–678.

9. Albert JS. Species diversity and phylogenetic systematics of American knifefishes (Gymnotiformes, Teleosti). Misc Publ Museum Zool Univ Michigan. University of Michigan Press; 2001;190: 1–140. 190

10. Lovejoy NR, Lester K, Crampton WGR, Marques FPL, Albert JS. Phylogeny, biogeography, and electric signal evolution of Neotropical knifefishes of the genus Gymnotus (Osteichthyes: Gymnotidae). Mol Phylogenet Evol. 2010;54: 278–90. doi: 10.1016/j.ympev.2009.09.017 19761855

11. Crampton WGR, Rodríguez-Cattáneo A, Lovejoy NR, Caputi AA. Proximate and ultimate causes of signal diversity in the electric fish Gymnotus. J Exp Biol. 2013;216: 2523–2541. doi: 10.1242/jeb.083261 23761477

12. Tagliacollo V, Bernt MJ, Craig JM, Oliviera C, Albert JS. Model-based Total Evidence phylogeny of Neotropical electric knifefishes (Ostariophysi, Gymnotiformes). Mol Phylogenet Evol. 2016;95: 20–33. doi: 10.1016/j.ympev.2015.11.007 26616344

13. Van der Sleen P, Albert JS. Field Guide to The Fishes of the Amazon, Orinoco, and Guianas. University of Princeton Press; 2017.

14. Ellis MM. The gymnotid eels of Tropical America. Mem Carnegie Museum. 1913;6: 109–195.

15. Bennett D, Hettling H, Silvestro D, Zizka A, Bacon C, Faurby S, et al. phylotaR: An Automated Pipeline for Retrieving Orthologous DNA Sequences from GenBank in R. Life. 2018;8: 20. doi: 10.3390/life8020020 29874797

16. Sanderson MJ, Boss D, Chen D, Cranston KA, Wehe A. The PhyLoTA Browser: Processing GenBank for molecular phylogenetics research. Syst Biol. 2008;57: 335–346. doi: 10.1080/10635150802158688 18570030

17. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215: 403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712

18. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005;33: 511–8. doi: 10.1093/nar/gki198 15661851

19. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25: 1972–1973. doi: 10.1093/bioinformatics/btp348 19505945

20. Guindon S, Dufayard J-FF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol. 2010;59: 307–321. doi: 10.1093/sysbio/syq010 20525638

21. Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T. GUIDANCE: A web server for assessing alignment confidence scores. Nucleic Acids Res. 2010;38: 23–28. doi: 10.1093/nar/gkq443 20497997

22. Albert JS, Crampton WGR, Thorsen DH, Lovejoy NR. Phylogenetic systematics and historical biogeography of the Neotropical electric fish Gymnotus (Teleostei: Gymnotidae). Syst Biodivers. 2005;2: 375–417. doi: 10.1017/S1477200004001574

23. Campos-da-Paz R. Gymnotus diamantinensis, a new species of electric knifefish from upper rio Arinos basin, Brazil (Ostariophysi: Gymnotidae). Ichthyol Explor Freshwaters. 2002;13: 185–192.

24. Campos-da-Paz R, Costa WJEM. Gymnotus bahianus sp. nov., a new gymnotid fish from eastern Brazil (Teleostei: Ostariophysi: Gymnotiformes), with evidence for the monophyly of the genus. Copeia. 1996;1996: 937–944.

25. Cognato D, Richer-de-Forges MM, Albert JS, Crampton WGR. Gymnotus chimarrao, a new species of electric fish (Gymnotiformes: Gymnotidae) from Southern Brazil. Ichthyol Explor Freshwaters. 2007;18: 375–382.

26. Crampton WGR, Lovejoy NR, Albert JS. Gymnotus ucamara: a new species of Neotropical electric fish from the Peruvian Amazon (Ostariophysi: Gymnotidae), with notes on ecology and electric organ. Zootaxa. 2003;277: 1–18. Available: http://www.researchgate.net/publication/228494257_Gymnotus_ucamara_a_new_species_of_Neotropical_electric_fish_from_the_Peruvian_Amazon_(Ostariophysi_Gymnotidae)_with_notes_on_ecology_and_electric_organ_

27. Crampton WGR, Albert JS. Redescription of Gymnotus coropinae (Gymnotiformes, Gymnotidae), an often misidentified species of Neotropical electric fish, with notes on natural history and electric signals. Zootaxa. 2003;348: 1–20.

28. Crampton WGR, Albert JS. Redescription of Gymnotus coatesi (Gymnotiformes, Gymnotidae): A Rare Species of Electric Fish from the Lowland Amazon Basin, with Descriptions of Osteology, Electric Signals, and Ecology. Copeia. 2004. pp. 525–533. doi: 10.1643/CI-03-246R1

29. Fernandes FM, Albert JS, Daniel-Silva MFZ, Lopes CE, Crampton WGR, Almeida-Toledo LF. A new Gymnotus (Teleostei: Gymnotiformes:Gymnotidae) from the Pantanal Matogrossense of Brazil and adjacent drainages: continued documentation of a cryptic fauna. Zootaxa. Magnolia Press; 2005;933: 1–14.

30. Giora J, Malabarba LR. Gymnotus refugio, a new and endangered species of electric fish of the Gymnotus pantherinus species-group from southern Brazil (Gymnotiformes: Gymnotidae). 2016;4066: 581–590. doi: 10.11646/zootaxa.4066.5.6 27395856

31. Hoedeman JJ. Notes on the ichthyology of Surinam and other Guianas. 9. New records of gymnotid fishes. Bull Aquat Biol. 3(26). Bull. Aq. Biol.; 1962;3: 53–60.

32. Linnaeus C. Systema Naturae Per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, Cum Charcteribus, Differentiis, Synonymis, Locis. Tomus I ED, editor. 1758.

33. Valenciennes A. Poissons. Catalogue des principales espèces de poissons, rapportées de l’Amérique méridionale. In: D’Orbigny A, editor. Voyage dans l’Amérique méridionale. Paris: Chez Pitois-Levrault; 1847. pp. 1–11.

34. Mago-Leccia F. Electric fishes of the continental waters of America. Vol. 29. Biblioteca de la Academia de Ciencias Fisicas, Matematicas y Naturales, Caracas, Venezuela; 1994.

35. Maldonado-Ocampo JA, Albert JS. Gymnotus ardilai: a new species of Neotropical electric fish (Ostariophysi: Gymnotidae) from the Rio Magdalena Basin of Colombia. Zootaxa. 2004;759: 1–10. Available: http://www.mapress.com/zootaxa/2004f/z00759f.pdf

36. Maxime EL, Albert JS. Redescription of the Tuvirão, Gymnotus inaequilabiatus Valenciennes, 1839, Using High-Resolution X-ray Computed Tomography. Copeia. 2014;14: 462–472. doi: 10.1643/CI-13-054

37. Maxime EL, Lima FCT, Albert JS. A New Species of Gymnotus (Gymnotiformes: Gymnotidae) from Rio Tiquié in Northern Brazil. Copeia. The American Society of Ichthyologists and Herpetologists 810 East 10th Street, P.O. Box 1897, Lawrence, Kansas 66044; 2011;1: 77–81. Available: http://www.asihcopeiaonline.org/doi/abs/10.1643/CI-10-009

38. Richer-de-Forges MM, Crampton WGR, Albert JS. A New Species of Gymnotus (Gymnotiformes, Gymnotidae) from Uruguay: Description of a Model Species in Neurophysiological Research. Copeia. The American Society of Ichthyologists and Herpetologists; 2009;2009: 538–544. doi: 10.1643/CI-07-103

39. Craig JM, Correa-roldán V, Ortega H, Crampton WGR, Albert JS. Revision of Gymnotus (Gymnotiformes: Gymnotidae) from the Upper Madeira Basin of Bolivia and Peru, with descriptions of two new species. Zootaxa. 2018;4413: 111–132. doi: 10.11646/zootaxa.4413.1.3 29690122

40. Milhomem SSR, Crampton WGR, Pieczarka JC, Shetka GH, Silva DS, Nagamachi CY. Gymnotus capanema, a new species of electric knife fish (Gymnotiformes, Gymnotidae) from eastern Amazonia, with comments on an unusual karyotype. J Fish Biol. 2012;80: 802–815. doi: 10.1111/j.1095-8649.2012.03219.x 22471800

41. Rangel-Pereira FS. Gymnotus capitimaculatus, a new species of electric fish from rio Jucuruçu basin, northeastern Brazil (Ostariophysi: Gymnotiformes: Gymnotidae). Vertebr Zool. 2014;64: 169–175. Available: http://www.senckenberg.de/files/content/forschung/publikationen/vertebratezoology/vz64-2/02_vertebrate_zoology_64-2_rangel-pereira_169-175.pdf

42. Rangel-Pereira FS. Gymnotus interruptus, a new species of eletric fish from the Rio de Contas basin, Bahia, Brazil (Teleostei: Gymnotiformes: Gymnotidae). Vertebr Zool. 2012;62: 363–370. Available: http://www.senckenberg.de/files/content/forschung/publikationen/vertebratezoology/vz62-3/03_vertebrate_zoology_62-3_rangel-pereira_363-370.pdf

43. Maxime EL, Albert JS. A new species of Gymnotus (Gymnotiformes: Gymnotidae) from the Fitzcarrald Arch of southeastern Peru. Neotrop Ichthyol. 2009;7: 579–585. doi: 10.1590/S1679-62252009000400004

44. Albert JS, de Campos Fernandes-Matioli FM, de Almeida-Toledo LF. New Species of Gymnotus (Gymnotiformes, Teleostei) from Southeastern Brazil: Toward the Deconstruction of Gymnotus carapo. Copeia. 1999;1999: 410–421. doi: 10.2307/1447486

45. Lanfear R, Calcott B, Ho SYW, Guindon S. Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol. 2012;29: 1695–701. doi: 10.1093/molbev/mss020 22319168

46. Bazinet AL, Zwickl DJ, Cummings MP. A gateway for phylogenetic analysis powered by grid computing featuring GARLI 2.0. Syst Biol. 2014;63: 812–818. doi: 10.1093/sysbio/syu031 24789072

47. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61: 539–42. doi: 10.1093/sysbio/sys029 22357727

48. Lewis PO. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol. 2001;50: 913–925. doi: 10.1080/106351501753462876 12116640

49. Sukumaran J, Holder MT. DendroPy: A Python library for phylogenetic computing. Bioinformatics. 2010;26: 1569–1571. doi: 10.1093/bioinformatics/btq228 20421198

50. Rambaut A, Drummond A. FigTree: Tree figure drawing tool, v1.4.4. Inst Evol Biol Univ Edinburgh. 2018;

51. Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30: 1312–1313. doi: 10.1093/bioinformatics/btu033 24451623

52. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science gateway. Proc Gatew Comput Environ Work. 2010;1: 1–7. Available: http://www.phylo.org/sub_sections/portal/sc2010_paper.pdf%0Afile:///Users/libbybeckman/Documents/Papers/2010/Miller/2010Miller.pdf%5Cnpapers://12c9fa01-b726-46f2-ab50-bd61d1a8ce24/Paper/p1475

53. Goloboff A P, Farris S J, Nixon C K. TNT, a free program for phylogenetic analysis. Cladistics. 2008;24: 774–786.

54. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, et al. BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Comput Biol. 2014;10: 1–6. doi: 10.1371/journal.pcbi.1003537 24722319

55. Albert JS, Lovejoy NR, Crampton WGR. Miocene tectonism and the separation of cis- and trans-Andean river basins: Evidence from Neotropical fishes. J South Am Earth Sci. 2006;21: 14–27. doi: 10.1016/j.jsames.2005.07.010

56. Rambaut A, Drummond A, Xie D, Biol GB-S, 2018 undefined. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. AcademicOupCom. 2018;00: 1–3. doi: 10.1093/sysbio/syy032/4989127 29718447

57. LaMonte FR. Two new species of Gymnotus. Publ Am Museum Nat Hist. 1935;781: 1–3.

58. Vanin AS, Giora J, Fialho CB. Life history of Gymnotus refugio (Gymnotiformes; Gymnotidae): an endangered species of weakly electric fish. Environ Biol Fishes. Environmental Biology of Fishes; 2016; 1–16. doi: 10.1007/s10641-016-0556-z

59. Burridge CP, Craw D, Waters JM. River capture, range expansion, and cladogenesis: the genetic signature of freshwater vicariance. Evolution. 2006;60: 1038–49. Available: http://www.ncbi.nlm.nih.gov/pubmed/16817543 16817543

60. Albert JS, Craig JM, Tagliacollo VA, Petry P. Upland and Lowland Fishes: A Test of the River Capture Hypothesis. In: Hoorn C, Perrigo A, Antonelli A, editors. Mountains, Climate and Biodiversity. 2018.

61. Antonelli A, Ariza M, Albert J, Andermann T, Azevedo J, Bacon C, et al. Conceptual and empirical advances in Neotropical biodiversity research. PeerJ. 2018;6: e5644. doi: 10.7717/peerj.5644 30310740

62. Albert JS, Petry P, Reis RE. Major biogeographic and phylogenetic patterns. In: Albert JS, Petry P, Reis RE, editors. Historical Biogeography of Neotropical Freshwater Fishes. Berkeley, CA; 2011.

63. Tagliacollo VA, Duke-Sylvester SM, Matamoros WA, Chakrabarty P, Albert JS. Coordinated dispersal and pre-isthmian assembly of the central American ichthyofauna. Syst Biol. 2017;66: 183–196. doi: 10.1093/sysbio/syv064 26370565

64. Lehmberg ES, Elbassiouny AA, Bloom DD, López-Fernández H, Crampton WGR, Lovejoy NR. Fish biogeography in the “Lost World” of the Guiana Shield: Phylogeography of the weakly electric knifefish Gymnotus carapo (Teleostei: Gymnotidae). J Biogeogr. 2018; 1–11. doi: 10.1111/jbi.13177

65. Albert JS, Val P, Hoorn C. The changing course of the Amazon River in the Neogene: center stage for Neotropical diversification. Neotrop Ichthyol. 2018;16: 1–24. doi: 10.1590/1982-0224-20180033

66. Correa SB, Crampton WGR, Chapman LJ, Albert JS. A comparison of flooded forest and floating meadow fish assemblages in an upper Amazon floodplain. J Fish Biol. 2008;72: 629–644. doi: 10.1111/j.1095-8649.2007.01752.x

67. Crampton WGR. Ecology and life history of an Amazon floodplain cichlid: The discus fish Symphysodon (Perciformes: Cichlidae). Neotrop Ichthyol. 2008;6: 599–612. doi: 10.1590/S1679-62252008000400008

68. Lundberg JG, Marshall LG, Guerrero J, Horton B, Malabarba MCSL, Wesselingh F. The stage for Neotropical fish diversification a history of tropical South American rivers. Phylogeny and classification of neotropical fishes. 1998. pp. 13–48.

69. Tagliacollo VA, Roxo FF, Duke-Sylvester SM, Oliveira C, Albert JS. Biogeographical signature of river capture events in Amazonian lowlands. J Biogeogr. 2015;42: 2349–2362. doi: 10.1111/jbi.12594

70. TN G. Ichthyological notes. Proc Acad Nat Sci Philidelphia. 1864;20: 151–154.

71. Houttuyn MB. Natuurlyke historie: of, Uitvoerige beschryving der dieren, planten, en mineraalen. Amsterdam: TE Amsterdam; 1764.

72. Chiaje S delle. Nuovi Annali delle Scienze naturali Bologna. Bologna; 1847.

73. Stocking Brown PS. Early women ichthyologists. Environ Biol Fishes. 1994;41: 9–32. doi: 10.1007/BF00023798

74. Fronk AH, Kim LY, Craig JM, Crampton WGR, Albert JS. Sexual Size Dimorphism in the Macana Tigrina, Gymnotus javari (Gymnotidae, Gymnotiformes). Copeia. 2019;107: 00. doi: 10.1643/CI-18-164

Phylogenetic revision of Gymnotidae (Teleostei: Gymnotiformes), with descriptions of six subgenera

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz