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Gracilaria caudata (Gracilariales, Rhodophyta) is reproductively compatible along the whole Brazilian coast

  • Amanda R. Chiaramonte
  • Paulo A. Parra
  • Lígia M. Ayres-Ostrock
  • Estela M. Plastino
VI REDEALGAS WORKSHOP (RIO DE JANEIRO, BRAZIL)

Abstract

Gracilaria spp. are economically important for the production of agar. The distribution of ecotypes of Gracilaria caudata all along the Brazilian coast raises questions regarding whether they are undergoing speciation and are possibly reproductively incompatible. Therefore, in the present work, we selected different female and male gametophytes of G. caudata from three populations along an extended Brazilian coastline (from 3° to 23° S) to perform crossing tests and observe possible reproductive barriers. In addition, we tested post-zygotic isolation, by following meiosis, the production of haploids, and the reproduction of haploids, in the progeny of these inter-population crosses. DNA sequences of the mitochondrial cytochrome c oxidase subunit 1 gene (COI) were used to determine relationships among all gametophytes employed in the crosses and to understand inheritance of mitochondria. The crosses showed interfertility between all populations tested. Neither pre- nor postzygotic isolation was seen in G. caudata from Brazil. Individuals with haplotypes that differ by 1–5 bp (0.15–0.79% divergences) in COI were reproductively compatible. In conclusion, the exchange of genetic material among populations from a wide geographic distribution allows consideration of G. caudata as a biological species.

Keywords

Crossing test Mitotype Mitochondrial inheritance COI Gracilaria Rhodophyta 

Notes

Acknowledgments

The authors acknowledge Rosário Petti for assistance on cultivation. We thank two anonymous reviewer for valuable comments on the manuscript.

Funding information

This research was supported by grants of the Brazilian National Council for Scientific and Technological Development (CNPq 300148/ 93-3, EMP; and 145966/2016-0, ARC) and São Paulo Research Foundation (FAPESP 2015/14893-2, LMAO).

Supplementary material

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ESM 1

Map of Brazilian coast showing the localities of sampled populations of G. caudata: Ceará (CE), Espírito Santo (ES), and São Paulo (SP) States. (PNG 15 kb)

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High Resolution Image (TIF 203 kb)
10811_2018_1642_Fig4_ESM.png (35 kb)
ESM 2

Maximum likelihood (ML) trees based on mitochondrial marker COI from distinct populations of Gracilaria caudata along the Brazilian coast. Bootstrap values for 2000 replicates are indicated on branches. Sequences from GenBank are followed by their accession number. New sequences produced in this study for COI are in boldface. Localities of G. caudata sampled: Ceará (CE), Rio Grande do Norte (RN), Pernambuco (PE), Bahia (BA), Espírito Santo (ES), São Paulo (SP), and Santa Catarina (SC) States. (PNG 35 kb)

10811_2018_1642_MOESM2_ESM.tif (3.2 mb)
High Resolution Image (TIF 3262 kb)

References

  1. Allendorf FW, Luikart GH, Aitken SN (2013) Conservation and the genetics of populations. Wiley-Blackwell, LondonGoogle Scholar
  2. Araújo FO, Ursi S, Plastino EM (2014) Intraspecific variation in Gracilaria caudata (Gracilariales, Rhodophyta): growth, pigment content, and photosynthesis. J Appl Phycol 26:849–858CrossRefGoogle Scholar
  3. Assis EA, Serrão O, Claro B, Perrin C, Pearson GA (2014) Climate-driven range shifts explain the distribution of extant gene pools and predict future loss of unique lineages in a marine brown alga. Mol Ecol 23:2797–2810CrossRefGoogle Scholar
  4. Ayres-Ostrock LM (2014) Population studies in Gracilaria birdiae and G. caudata (Gracilariales, Rhodophyta): phenological, physiological and molecular aspects. Thesis. University of São PauloGoogle Scholar
  5. Ayres-Ostrock LM, Mauger S, Plastino EM, Oliveira MC, Valero M, Destombe C (2016) Development and characterization of microsatellite markers in two agarophyte species, Gracilaria birdiae and Gracilaria caudata (Gracilariaceae, Rhodophyta), using next generation sequencing. J Appl Phycol 28:653–662CrossRefGoogle Scholar
  6. Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335CrossRefGoogle Scholar
  7. Carneiro MA, Marinho-Soriano E, Plastino EM (2011) Phenology of an agarophyte Gracilaria birdiae Plastino and EC Oliveira (Gracilariales, Rhodophyta) in northeastern Brazil. Rev bras farmacogn 21:317–322CrossRefGoogle Scholar
  8. Choi SJ, Park EJ, Endo H, Kidade Y, Saga N (2008) Inheritance pattern of chloroplast and mitochondrial genomes in artificial hybrids of Porphyra yezoensis (Rhodophyta). Fish Sci 74:822–829CrossRefGoogle Scholar
  9. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  10. Costa E, Plastino EM, Petti R, Oliveira EC, Oliveira MC (2012) The Gracilariaceae germplasm bank of the University of São Paulo, Brazil - a DNA barcoding approach. J Appl Phycol 24:1643–1653CrossRefGoogle Scholar
  11. Destombe C, Valero M, Guillemin ML (2010) Delineation of two sibling red algal species, Gracilaria gracilis and Gracilaria dura (Gracilariales, Rhodophyta), using multiple DNA markers: resurrection of the species G. dura previously described in the northern Atlantic 200 years ago. J Phycol 46:720–727CrossRefGoogle Scholar
  12. Faria AV, Plastino EM (2016) Physiological assessment of the mariculture potential of a Gracilaria caudata (Gracilariales, Rhodophyta) variant. J Appl Phycol 28:2445–2452CrossRefGoogle Scholar
  13. Faria AV, Bonomi-Barufi J, Plastino EM (2017) Ecotypes of Gracilaria caudata (Gracilariales, Rhodophyta): physiological and morphological approaches considering life history phases. J Appl Phycol 29:707–719CrossRefGoogle Scholar
  14. Guimarães MA, Coutinho R (2000) Temporal and spatial variation of Ulva spp. and water properties in the Cabo Frio upwelling region of Brazil. Aquat Bot 66:101–114CrossRefGoogle Scholar
  15. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  16. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefGoogle Scholar
  17. Hayashi L, Bulboa C, Kradolfer P, Soriano G, Robledo D (2014) Cultivation of red seaweeds: a Latin American perspective. J Appl Phycol 26:719–727CrossRefGoogle Scholar
  18. Kain JM, Destombe C (1995) A review of the life history, reproduction and phenology of Gracilaria. J Appl Phycol 7:269–281CrossRefGoogle Scholar
  19. Kalyaannamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estmates. Nature 14:587–589Google Scholar
  20. Li Q, Wang X, Zhang J, Yao J, Duan D (2016) Maternal inheritance of organellar DNA demonstrated with DNA markers in crosses of Saccharina japonica (Laminariales, Phaeophyta). J Appl Phycol 28:2019–2026CrossRefGoogle Scholar
  21. Lyra GDM, Costa EDS, Jesus PB, Matos JCG, Caires TA, Oliveira MC, Oliveira EC, Xi Z, Nunes JM, Davis CC (2015) Phylogeny of Gracilariaceae (Rhodophyta): evidence from plastid and mitochondrial nucleotide sequences. J Phycol 51:356–366CrossRefGoogle Scholar
  22. Maggs CA, Fletcher HL, Fewer D, Loade L, Mineur F, Johnson MP (2011) Speciation in red algae: members of the Ceramiales as model organisms. Integr Comp Biol 51:492–504CrossRefGoogle Scholar
  23. Mayr E (1992) A local flora and the biological species concept. Am J Bot 79:222–238CrossRefGoogle Scholar
  24. Minh BQ, Nguyen MAT, Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195CrossRefGoogle Scholar
  25. Montecinos AE, Guillemin ML, Couceiro L, Peters AF, Stoeckel S, Valero M (2017) Hybridization between two cryptic filamentous brown seaweeds along the shore: analyzing pre-and postzygotic barriers in populations of individuals with varying ploidy levels. Mol Ecol 26:3497–3512CrossRefGoogle Scholar
  26. Muangmai N, Fraser CI, Zuccarello GC (2015) Contrasting patterns of population structure and demographic history in cryptic species of Bostrychia intricata (Rhodomelaceae, Rhodophyta) from New Zealand. J Phycol 51:574–585CrossRefGoogle Scholar
  27. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2014) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274CrossRefGoogle Scholar
  28. Oliveira EC, Miranda GD (1998) Aspectos sociais e econômicos da explotação de algas marinhas no Brasil. In Anais do IV Congresso Latino-Americano, II Reunião Ibero-Americana, VII Reunião Brasileira de Ficologia, pp 149–156Google Scholar
  29. Oliveira EC, Plastino EM (1984) The life history of some species of Gracilaria (Rhodophyta) from Brazil. Jap J Phycol 32:203–208Google Scholar
  30. Oliveira EC, Alveal K, Anderson R (2000) Mariculture of the agar producing gracilarioid red algae. Rev Fish Sci 8:345–378CrossRefGoogle Scholar
  31. Plastino EM, Oliveira EC (1988) Sterility barriers among species of Gracilaria (Rhodophyta, Gigartinales) from the São Paulo Littoral, Brazil. Br Phycol J 23:267–271CrossRefGoogle Scholar
  32. Plastino EM, Oliveira EC (1990) Crossing experiments as an aid to the taxonomic recognition of the agarophytes Gracilaria. In: Oliveira EC, Kautsky N (eds) Cultivation of seaweeds in Latin America. Universidade de São Paulo, São Paulo, pp 127–133Google Scholar
  33. Plastino EM, Oliveira EC (1996) Approaches to the identification of terete Brazilian Gracilariaceae (Gracilariales, Rhodophyta). Hydrobiologia 326/327:145–148CrossRefGoogle Scholar
  34. Plastino EM, Oliveira EC (1997) Gracilaria caudata J. Agardh (Gracilariales, Rhodophyta)-restoring an old name for a common western Atlantic alga. Phycologia 36:225–232CrossRefGoogle Scholar
  35. Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Change 3:919–925CrossRefGoogle Scholar
  36. Porse H, Rudolph B (2017) The seaweed hydrocolloid industry: 2016 updates, requirements, and outlook. J Appl Phycol 29:2187–2200CrossRefGoogle Scholar
  37. Robba L, Russell SJ, Barker GL, Brodie J (2006) Assessing the use of mitochondrial cox1 marker for use in DNA barcoding of red algae (Rhodophyta). Am J Bot 93:1101–1108CrossRefGoogle Scholar
  38. Rodrigues RR, Lorenzetti JA (2001) A numerical study of the effects of bottom topography and coastline geometry on the southeast Brazilian coastal upwelling. Cont Shelf Res 21:377–394CrossRefGoogle Scholar
  39. Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Phil Trans R Soc Lond B 360:1879–1888CrossRefGoogle Scholar
  40. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  41. Ursi S, Plastino EM (2001) Crescimento in vitro de linhagens de coloração vermelha e verde clara de Gracilaria sp. (Gracilariales, Rhodophyta) em dois meios de cultura: análise de diferentes estádios reprodutivos. Rev Bras Bot 24:587–594CrossRefGoogle Scholar
  42. West JA, Polanshek AR, Shelvin DE (1978) Field and culture studies on Gigartina agardhii (Rhodophyta). J Phycol 14:416–426CrossRefGoogle Scholar
  43. Yow YY, Lim PE, Phang SM (2011) Genetic diversity of Gracilaria changii (Gracilariaceae, Rhodophyta) from west coast, Peninsular Malaysia based on mitochondrial cox1 gene analysis. J Appl Phycol 23:219–226CrossRefGoogle Scholar
  44. Zuccarello G, Sandercock B, West J (2002) Diversity within red algal species: variation in world-wide samples of Spyridia filamentosa (Ceramiaceae) and Murrayella periclados (Rhodomelaceae) using DNA markers and breeding studies. Eur J Phycol 37:403–417CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Departamento de Botânica, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil

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