Abstract
A significant portion of the threatened ichthyofauna is composed by annual fish, whose gene flow is commonly affected by large water bodies. Austrolebias minuano is an endangered species that lives in temporary wetlands of the Patos-Mirim Lagoon System, in Brazil, inhabiting both margins of the Patos Lagoon. This species has previously been target of taxonomic split, leading to the description of A. pongondo, and there are doubts about its distinction in relation to A. charrua. The objective of this study is to understand the evolutionary patterns and processes associated with the geographic distribution of A. minuano, A. charrua and A. pongondo, while assessing their taxonomic status. For this, specimens were collected along the distribution range of the three species, and sequences of the mitochondrial cyt b and CO1 and of the nuclear ENC1 gene were characterized. Phylogenetic and phylogeographic approaches showed subdivision of the dataset in four lineages: one clustering the type population of A. minuano with A. charrua, two presenting populations previously assigned to A. minuano that inhabit the Eastern margin of the Patos Lagoon and one corresponding to A. pongondo. Patterns of migration and genetic divergences support the assignment of each of these lineages as independent evolutionary units. In the chronophylogenetic reconstructions, the two lineages inhabiting the Western margin of the Patos Lagoon constituted the first to branch out whereas the eastern lineages diverged more recently. These divergences seem to have occurred before the Pleistocene Lagoon-Barrier Depositional System related to the paleogeographic evolution of the South American Coastal Plain.
Similar content being viewed by others
References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723. https://doi.org/10.1109/TAC.1974.1100705
Alonso F, Calviño P, Terán GE, García I (2016) Geographical distribution of Austrolebias monstrosus (Huber, 1995), A. elongatus (Steindachner, 1881) and A. vandenbergi (Huber, 1995) (Teleostei: Cyprinodontiformes), with comments on the biogeography and ecology of Rivulidae in Pampasic and Chaco floodp. Check List 12:1–7. https://doi.org/10.15560/12.4.1945
Alonso F, Terán GE, Calviño P, García I, Cardoso Y, García G (2018) An endangered new species of seasonal killifish of the genus Austrolebias (Cyprinodontiformes: Aplocheiloidei) from the Bermejo River basin in the Western Chacoan region. PLoS One 13:1–20. https://doi.org/10.1371/journal.pone.0196261
Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV (2012) Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29(9):2157–2167. https://doi.org/10.1093/molbev/mss084
Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Bartáková V, Reichard M, Janko K, Polačik M, Blažek R, Reichwald K, Cellerino A, Bryja J (2013) Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique. BMC Evol Biol 13:196. https://doi.org/10.1186/1471-2148-13-196
Bartáková V, Reichard M, Blažek R, Polačik M, Bryja J (2015) Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna. J Biogeogr 42:1832–1844. https://doi.org/10.1111/jbi.12567
Beerli P, Mashayekhi S, Sadeghi M, Khodaei M, Shaw K (2019) Population genetic inference with MIGRATE. Cur Prot Bioinf 68:e87. https://doi.org/10.1002/cpbi.87
Beheregaray L, Attard C, Brauer C, Hammer M (2016) Innovations in conservation: how genetics can help save freshwater fishes. Wildl Aust 53:34–37
Berois N, García G, de Sá R (2015) Annual fishes: life history strategy, diversity, and evolution. Taylor & Francis Group, New York
Bossi J, Navarro R (1988) Geología del Uruguay. Universidad de la República, Montevideo, 966 p
Brown WM, Jr George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A 76:1967–1971. https://doi.org/10.1073/pnas.76.4.1967
Corander J, Sirén J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129. https://doi.org/10.1007/s00180-007-0072-x
Costa WJEM (2006) The south American annual killifish genus Austrolebias (Teleostei: Cyprinodontiformes: Rivulidae): phylogenetic relationships, descriptive, morphology and taxonomic revision. Zootaxa 1213:1–162
Costa WJEM, Amorim PF (2011) A new annual killifish species of the Hypsolebias flavicaudatus complex from the são Francisco river basin, Brazilian Caatinga (Cyprinodontiformes: Rivulidae). Vertebr Zool 61:99–104
Costa WJEM, Cheffe MM (2001) Three new annual fishes of the genus Austrolebias from the Laguna dos Patos system, southern Brazil, and a redescription of A. adloffi (Ahl) (Cyprinodontiformes: Rivulidae). Comun do Mus Ciências e Tecnol da PUCRS. Série Zool 14:179–200
Costa WJEM, Cheffe MM, Amorim PF (2017) Two new seasonal killifishes of the Austrolebias adloffi group from the Lagoa dos Patos basin, southern Brazil (Cyprinodontiformes: Aplocheilidae). Vertebr Zool 67:139–149
Darriba D, Taboada G, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
de Sá RO, Berois N, García G (2015) Overview, future challenges, and evolution of Annualism. In: Berois N, García G, de Sá RO (eds) Annual fishes: life history strategy, diversity, and evolution, 1rd edn. Press Taylor & Francis group, Boca Raton, pp 309–318
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581. https://doi.org/10.1046/j.1365-294X.2002.01650.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fairley TL, Póvoa MM, Conn JE (2002) Evaluation of the Amazon River delta as a barrier to gene flow for the regional malaria vector, Anopheles aquasalis (Diptera: Culicidae) in northeastern Brazil. J Med Entomol 39:861–869. https://doi.org/10.1603/0022-2585-39.6.861
Fontana CS, Bencke GA, Reis RE (2003) Livro vermelho da fauna ameaçada de extinção no Rio Grande do Sul. Edipucrs, Porto Alegre
Freeland J (2005) Molecular ecology. John Wiley & Sons.
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Furness AI (2016) The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause. Biol Rev Camb Philos Soc 91:796–812. https://doi.org/10.1111/brv.12194
Garcez DK, Barbosa C, Loureiro M, Volcan MV, Loebmann D, Quintela FM, Robe LJ (2018) Phylogeography of the critically endangered neotropical annual fish, Austrolebias wolterstorffi (Cyprinodontiformes: Aplocheilidae): genetic and morphometric evidence of a new species complex. Environ Biol Fish 101:1503–1515. https://doi.org/10.1007/s10641-018-0795-2
Garcez DK, Fernandes MO, Ozório GR, Volcan MV, Robe LJ (2020) Phylogenetic structure of Neotropical annual fish of the genus Cynopoecilus Regan 1912 (Cyprinodontiformes: Rivulidae), with an assessment of taxonomic implications. J Zool Syst Evol Res 58:1123–1134. https://doi.org/10.1111/jzs.12389
García G, Wlasiuk G, Lessa EP (2000) High levels of mitochondrial cytochrome b divergence and phylogenetic relationships in the annual killifishes ofthe genus Cynolebias (Cyprinodontiformes, Rivulidae). Zool J Linnean Soc 129:93–110. https://doi.org/10.1006/zjls.1999.0202
García G, Gutiérrez V, Vergara J, Calviño P, Duarte A, Loureiro M (2012) Patterns of population differentiation in annual killifishes from the Paraná-Uruguay-La Plata basin: the role of vicariance and dispersal. J Biogeogr 39:1707–1719. https://doi.org/10.1111/j.1365-2699.2012.02722.x
García G, Gutiérrez V, Ríos N, Turner B, Santiñaque F, López-Carro B, Folle G (2014) Burst speciation processes and genomic expansion in the neotropical annual killifish genus Austrolebias (Cyprinodontiformes, Rivulidae). Genetica 142:87–98. https://doi.org/10.1007/s10709-014-9756-7
García G, Gutiérrez V, Ríos N, de Sá RO (2015a) Comparative Phylogeographic patterns in Austrolebias from different south American basins. In: Berois N, García G, de Sá RO (eds) Annual fishes: life history strategy, diversity, and evolution, 1rd edn. Press Taylor & Francis group, Boca Raton, pp 259–279
García G, Ríos N, Gutiérrez V (2015b) Next-generation sequencing detects repetitive elements expansion in giant genomes of annual killifish genus Austrolebias (Cyprinodontiformes, Rivulidae). Genetica 143:353–360. https://doi.org/10.1007/s10709-015-9834-5
García G, Gutierrez V, Rios N, Papa N, Serra S, Loureiro M (2020) Characterization of a hybrid zone between two annual killifish genus Austrolebias from the biosphere reserve and Ramsar sites in South America. Hydrobiologia 847(2):421–442. https://doi.org/10.1007/s10750-019-04104-0
Haffer JR (1997) Alternative models of vertebrate speciation in Amazonia: an overview. Biodivers Conserv 6:451–476. https://doi.org/10.1023/A:1018320925954
Hayes FE, Sewlal JAN (2004) The Amazon River as a dispersal barrier to passerine birds: effects of river width, habitat and taxonomy. J Biogeogr 31:1809–1818. https://doi.org/10.1111/j.1365-2699.2004.01139.x
ICMbio (2018) Plano de Ação Nacional para a Conservação dos Peixes Rivulídeos Ameaçados de Extinção. http://www.icmbio.gov.br/portal/faunabrasileira/plano-de-acao-nacional-lista/2833-plano-de-acao-nacional-para-a-conservacao-dos-rivulideos. Accessed 20 Aug 2018
Jowers MJ, Cohen BL, Downie JR (2008) The cyprinodont fish Rivulus (Aplocheiloidei: Rivulidae) in Trinidad and Tobago: molecular evidence for marine dispersal, genetic isolation and local differentiation. J Zool Syst Evol Res 46:48–55. https://doi.org/10.1111/j.1439-0469.2007.00422.x
Li C, Ortí G, Zhang G, Lu G (2007) A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evol Biol 7:1–11. https://doi.org/10.1186/1471-2148-7-44
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Loureiro M, Borthagaray A, Hernández D, Duarte A, Pinelli V, Arim M (2015) Austrolebias in space: scaling from ponds to biogeographical regions. In: Berois N, García G, de Sá RO (eds) Annual fishes: life history strategy, diversity, and evolution, 1rd edn. Press Taylor & Francis group, Boca Raton, pp 111–132
Loureiro M, de Sá RO, Serra W, Alonso F, Nielsen D, Calviño P, Volcan MV, Lanés LE, Duarte A, García G (2018) Review of the family Rivulidae (Cyprinodontiformes, Aplocheiloidei) and a molecular and morphological phylogeny of the annual fish genus Austrolebias Costa 1998. Neotrop Ichthyol 16(3):e180007. https://doi.org/10.1590/1982-0224-20180007
Matioli SR, Fernandes FMC (2012) Biologia molecular e evolução. Holos, São Paulo
Nielsen DTB, Pillet D (2015) Austrolebias accorsii, a new annual fish (Cyprinodontiformes: Rivulidae: Cynolebiatinae) from the upper Río Grande basin, Amazon basin, Bolivia, Aqua. Int J Ichthyol 21(4):172–179
Nores M (2000) Species richness in the Amazonian bird fauna from an evolutionary perspective. Emu 100:419–430. https://doi.org/10.1071/MU0007S
Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. University of Hawaii, Honolulu
Patton JL, Da Silva MNF, Malcolm JR (1994) Gene genealogy and differentiation among arboreal spiny rats (Rodentia: Echimyidae) of the Amazon basin: a test of the riverine barrier hypothesis. Evolution 48:1314–1323. https://doi.org/10.1111/j.1558-5646.1994.tb05315.x
Ponce de León JL, León G, Rodríguez R, Metcalfe CJ, Hernández D, Casane D, García-Machado E (2014) Phylogeography of Cuban Rivulus: evidence for allopatric speciation and secondary dispersal across a marine barrier. Mol Phylogenet Evol 79:404–414. https://doi.org/10.1016/j.ympev.2014.07.007
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Molecular evolution, phylogenetics and epidemiology. In: Tracer v1.7. http://tree.bio.ed.ac.uk/software/tracer/. Accessed 28 Aug 2018
Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102. https://doi.org/10.1146/annurev.ecolsys.38.091206.095733
Ronquist F, Teleslenko M, Van Der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:1–4. https://doi.org/10.1093/sysbio/sys029
Rosa RS, Lima FCT (2008) Peixes. Ministério do Meio Ambiente, Brasília
Sambrook J, Fritschi EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harb Lab Press, New York
Sedláček O, Baciaková B, Kratochvíl L (2014) Evolution of body colouration in killifishes (Cyprinodontiformes: Aplocheilidae, Nothobranchiidae, Rivulidae): is male ornamentation constrained by intersexual genetic correlation? Zool Anz 253:207–215. https://doi.org/10.1016/j.jcz.2013.12.004
Rio Grande do Sul (2014) Decreto no 51.797 - Declara as Espécies da Fauna Silvestre Ameaçadas de Extinção no Estado do Rio Grande do Sul. DOE 173. https://www.al.rs.gov.br/filerepository/repLegis/arquivos/DEC%2051.797.pdf. Accessed Nov 2020
Serra WS, Loureiro M (2018) Austrolebias queguay (Cyprinodontiformes, Rivulidae), a new species of annual killifish endemic to the lower Uruguay river basin. Zoosyst Evol 94:547–556. https://doi.org/10.3897/zse.94.29115
Staden R (1996) The Staden sequence analysis package. Appl Biochem Biotechnol Part B Mol Biotechnol 5:233–241. https://doi.org/10.1007/BF02900361
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics alanysis version 6.0. Mol Biol Evol 30:2725–2729
Vallinoto M, Araripe J, Rego PSD, Tagliaro CH, Sampaio I, Schneider H (2006) Tocantins river as an effective barrier to gene flow in Saguinus niger populations. Genet Mol Biol 29:215–219. https://doi.org/10.1590/S1415-47572006000200005
Villwock JA, Tomazelli LJ (2007) Planície Costeira do Rio Grande do Sul: gênese e paisagem atual. In: Becker FG, Ramos RA, Moura LA (ed) Biodiversidade. Regiões da Lagoa do Casamento e dos Butiazais de Tapes, planície costeira do Rio Grande do Sul. MMA/SBF, Brasília, pp 20-33
Volcan MV, Severo-Neto F (2019) Austrolebias ephemerus (Cyprinodontiformes: Rivulidae), a new annual fish from the upper Rio Paraguai basin, Brazilian Chaco. Zootaxa 4560(3):541–553. https://doi.org/10.11646/zootaxa.4560.3.6
Volcan MV, Lanés LEK, Gonçalves ÂC (2014) Austrolebias bagual, a new species of annual fish (Cyprinodontiformes: Rivulidae) from southern Brazil. Int J Ichthyol 20:161–172
Volcan MV, Lanés LEK, Gonçalves ÂC, Guadagnin DL (2015) Annual fishes (Rivulidae) from southern Brazil: a broad-scale assessment of their diversity and conservation. In: Berois N, García G, de Sá RO (eds) Annual fishes: life history strategy, diversity, and evolution, 1rd edn. Press Taylor & Francis group, Boca Raton, pp 185–203
Weschenfelder J, Correa ICS, Aliotta S, Baitelli R (2010) Paleochannels related to late Quaternary Sea-level changes in southern Brazil. Braz J Oceanogr 58:35–44
Wolf C (1999) PCR-RFLP analysis of mitochondrial DNA: a reliable method for species identification. J Agric Food Chem 47:1350–1355. https://doi.org/10.1021/jf9808426
Acknowledgements
This study was funded by Fundação Grupo Boticário de Proteção à Natureza as part of the project “Padrões micro e macroevolutivos em peixes anuais de Cynopoecilus e Austrolebias (Cyprinodontiformes: Rivulidae) ao longo do Sistema de Drenagens Patos-Mirim: um enfoque comparativo com aplicações para a conservação – 1090_20171”. LJR and ASVJ are research fellows of the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (#308371/2018-6 and 310327/2018-0, respectively). We also thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 for providing fellowships to MOF, DKG and CB. This study was approved by the Ethics Committee for Animal Use of Federal University of Rio Grande (CEUA-FURG, permission number: 23116.008163/2015-23).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Fig. 1S
Majority-rule consensus tree recovered by MrBayes 3.2.6 for sequences of cyt b (A), CO1 (B), the concatenated mitochondrial dataset (C) and ENC1 (D). Values above the branches represent support values, as measured by the posterior probabilities of each clade. Lineages were collapsed and represented by their respective names and colors, as given in Fig. 1. Numbers within parenthesis to the right of the image represent sample sizes. The phylogenies were rooted with sequences of A. wolterstorffi, which were later omitted from the topology (PNG 389 kb)
Fig. 2S
Structure of population subdivision recovered by BAPS 6 for cyt b (A), the concatenated mitochondrial dataset (B) and ENC1 (C) as a function of the geographic coordinates of each population. Each color represents a different cluster, to the exception of yellow and green, which represent the populations of A. minuano and A. charrua, respectively, which together encompass the lineage named A. minuano / A. charrua. Red, blue and purple refer to the clusters of A. minuano affinis 1, A. minuano affinis 2 and A. pongondo, respectively, and brown depict populations groups that join two or more of the four lineages recovered in this study (PNG 452 kb)
ESM 1
(DOCX 66 kb)
Rights and permissions
About this article
Cite this article
de Oliveira Fernandes, M., Barbosa, C., Garcez, D.K. et al. Phylogeographic analyses and taxonomic inconsistencies of the Neotropical annual fish Austrolebias minuano, Austrolebias charrua and Austrolebias pongondo (Cyprinodontiformes: Rivulidae). Environ Biol Fish 104, 1–14 (2021). https://doi.org/10.1007/s10641-020-01045-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-020-01045-9