Skip to main content
SpringerLink
Log in

The Experimental Heterochronies in a Green Terror Cichlid Andinoacara rivulatus (Teleostei: Cichlidae: Cichlasomatinae) Indicate a Role of Developmental Changes in the Cichlids Coloration Evolution

  • CONFERENCE MATERIALS
  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

Cichlids (Teleostei; Cichlidae) display a high variability of coloration, a morphological characteristic playing an important role in the life and evolution of fishes. The heterochrony—alterations in the developmental timing and rate—has been suggested to be one of the key mechanisms underpinning evolution of the pigment patterns in cichlids. Here, we present the experimental data indicating that heterochronies have an important role to play in the diversification of the American cichlids coloration. The data were obtained in the experiments with the green terror cichlid, Andinoacara rivulatus (Cichlasomatinae). The experimental heterochronies were induced by the manipulations with the level of the thyroid hormones, the crucial regulators of the developmental rate and timing in the lower vertebrates. We revealed: (i) the adult coloration of A. rivulatus is determined by the timing and rate of the pigment patterning; and (ii) the experimental heterochronies result in the appearance of the phenotypes mimicking the phenotypes typical of the various Cichlasomatinae species. These findings support the hypothetical role of heterochronies in the evolution of the American cichlids color pattern. Moreover, the revealed dependence of the cichlids pigment patterning on the thyroid axis activity offers the prospect for studying the role of the endocrine system in the evolution of bony fishes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Aranda, A. and Pascual, A., Nuclear hormone receptors and gene expression, Physiol. Rev., 2001, vol. 81, pp. 1269–1304.

    Article  CAS  PubMed  Google Scholar 

  2. Barluenga, M., Stölting, K.N., Salzburger, W., Muschick, M., and Meyer, A., Sympatric speciation in Nicaraguan crater lake cichlid fish, Nature, 2006, vol. 439, pp. 719–723.

    Article  CAS  PubMed  Google Scholar 

  3. Bassett, J.D., Harvey, C.B., and Williams, G.R., Mechanisms of thyroid hormone receptor-specific nuclear and extra nuclear actions, Mol. Cell. Endocrinol., 2003, vol. 213, pp. 1–11.

    Article  CAS  PubMed  Google Scholar 

  4. Bird, N.C. and Webb, J.F., Heterochrony, modularity, and the functional evolution of the mechanosensory lateral line canal system of fishes, EvoDevo, 2014, vol. 5, p. 21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Blanton, M.L. and Specker, J.L., The hypothalamic–pituitary–thyroid (HPT) axis in fish and its role in fish development and reproduction, Critical Rev. Toxicol., 2007, vol. 37, pp. 97–115.

    Article  CAS  Google Scholar 

  6. Bolotovskiy, A.A. and Levin, B.A., Effects of thyroid hormones on vertebral numbers in two cyprinid fish species: Rutilus rutilus (Linnaeus, 1758) and Abramis brama (Linnaeus, 1758), J. Appl. Ichthyol., 2018, pp. 1–6.

    Google Scholar 

  7. Bolotovskiy, A.A., Levina, M.A., DeFaveri, J., Merila, J., and Levin, B.A., Heterochronic development of lateral plates in the three-spined stickleback induced by thyroid hormone level alterations, PLoS One, 2018, vol. 13. e0194040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Brawand, D., Wagner, C.E., Li, Y.I., Malinsky, M., Keller, I., Fan, S., Simakov, O., Alvin, Y., Ng, A.Y., Lim, Z.W., Bezault, E., Turner-Maier, J., Johnson, J., Alcazar, R., Noh, H.J., Russell, P., Aken, B., Alfoldi, J., Amemiya, C., Azzouzi, N., Baroiller, J., Barloy-Hubler, F., Berlin, A., Bloomquist, R., Carleton, K., Conte, M.A., D’Cotta, H., Eshel, O., Gaffney, L., Galibert, F., Gante, H.F., Gnerre, S., Greuter, L., Guyon, R., Haddad, N.S., Haerty, W., Harris, R.M., Hofmann, H.A., Hourlier, T., Hulata, G., Jaffe, D.B., Lara, M., Lee, A.P., MacCallum, I., Mwaiko, S., Nikaido, M., Nishihara, H., Ozouf-Costaz, C., Penman, D.J., Przybylski, D., Rakotomanga, M., Renn, S., Ribeiro, F.J., Ron, M., Salzburger, W., Sanchez-Pulido, L., Santos, M.E., Searle, S., Sharpe, T., Swofford, R., Tan, F.J., Williams, L., Young, S., Yin, S., Okada, N., Kocher, T.D., Miska, E.A., Lander, E.S., Venkatesh, B., Fernald, R.D., Meyer, A., Ponting, C.P. Streelman, J.T., Lindblad-Toh, K., Seehausen, O., and Palma, F.D., The genomic substrate for adaptive radiation in African cichlid fish, Nature, 2014, vol. 513, pp. 375–381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Brent, G.A., Mechanisms of thyroid hormone action, J. Clin. Invest., 2012, vol. 122, pp. 3035–3043.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Brown, D.D., The role of thyroid hormone in zebrafish and axolotl development, Proc. Natl. Acad. Sci. U. S. A., 1997, vol. 9, pp. 13011–13016.

    Article  Google Scholar 

  11. Cheng, S.Y., Leonard, J.L., and Davis, P.J., Molecular aspects of thyroid hormone actions, Endocrine Rev., 2010, vol. 31, pp. 139–170.

    Article  CAS  Google Scholar 

  12. Dittmann, M.T., Roesti, M., Indermaur, A., Colombo, M., Gschwind, M., Keller, I., Kovac, R., Barluenga, M., Muschick, M., and Salzburger, W., Depth-dependent abundance of Midas Cichlid fish (Amphilophus spp.) in two Nicaraguan crater lakes, Hydrobiologia, 2012, vol. 686, pp. 277–285.

    Article  Google Scholar 

  13. Elmer, K.R., Fan, S., Kusche, H., Spreitzer, M.L., Kautt, A.F., Franchini, P., and Meyer, A., Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes, Nat. Comm., 2014, vol. 5 P, p. 168.

  14. Guillot, R., Muriach, B., Rocha, A., Rotllant, J., Kelsh, R.N., and Cerdá-Reverter, J.M., Thyroid hormones regulate zebrafish melanogenesis in a gender-specific manner, PLoS One, 2016, vol. 11. e0166152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hulbert, A.J., Thyroid hormones and their effects: a new perspective, Biol. Rev., 2000, vol. 75, pp. 519–631.

    Article  CAS  PubMed  Google Scholar 

  16. Hulsey, C.D., Hollingsworth, P.R., and Fordyce, J.A., Temporal diversification of Central American cichlids, BMC Evol. Biol., 2010, vol. 10, p. 279.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Jegstrup, I.M. and Rosenkilde, P., Regulation of post-larval development in the European eel: thyroid hormone level, progress of pigmentation and changes in behavior, J. Fish. Biol., 2003, vol. 63, pp. 168–175.

    Article  CAS  Google Scholar 

  18. de Jesus, E.G.T., Toledo, J.D., and Simpas, M.S., Thyroid hormones promote early metamorphosis in grouper (Epinephelus coioides) larvae, General Comp. Endocrinol., 1998, vol. 112, pp. 10–16.

    Article  CAS  Google Scholar 

  19. Koblmüller, S., Albertson, R.C., Genner, M.J., et al., Preface: advances in cichlid research II: behavior, ecology and evolutionary biology, Hydrobiologia, 2017, vol. 791, pp. 1–6.

    Article  Google Scholar 

  20. Levin, B.A., Drastic shift in the number of lateral line scales in the common roach Rutilus rutilus as a result of heterochronies: experimental data, J. Appl. Ichthyol., 2010, vol. 26, pp. 303–306.

    Article  Google Scholar 

  21. López-Fernández, H., Winemiller, K.O., and Honeycutt, R.L., Multilocus phylogeny and rapid radiations in Neotropical cichlid fishes (Perciformes: Cichlidae: Cichlinae), Mol. Phylogenet. Evol., 2010, vol. 55, pp. 1070–1086.

    Article  PubMed  Google Scholar 

  22. Martin, C.H., Cutler, J.S., Friel, J.P., Touokong, C.D., Coop, G., and Wainwright, P.C., Complex histories of repeated gene flow in Cameroon crater lake cichlids cast doubt on one of the clearest examples of sympatric speciation, Evolution, 2015, vol. 69, pp. 1406–1422.

    Article  PubMed  Google Scholar 

  23. McCrary, J., The arrow cichlid, Amphilophus zaliosus, of Lake Apoyo, Nicaragua, Cichlid News, 2015, vol. 24, no. 1.

  24. McMenamin, S.K. and Parichy, D.M., Metamorphosis in teleosts, Curr. Top. Dev. Biol., 2013, vol. 103, pp. 127–165.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. McMenamin, S.K., Bain, E.J., McCann, A.E., Patterson, L.B., Eom, D.S., Waller, Z.P., Hamill, J.C., Kuhlman, J.A., Eisen, J.S., and Parichy, D.M., Thyroid hormone-dependent adult pigment cell lineage and pattern in zebrafish, Science, 2014, vol. 345, pp. 1358–1361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. McMenamin, S.K., Carter, C., and Cooper, W.J., Thyroid hormone stimulates the onset of adult feeding kinematics in zebrafish, Zebrafish, 2017, vol. 14, pp. 517–525.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Meyer, A., Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes, Evolution, 1987, vol. 41, pp. 1357–1369.

    PubMed  Google Scholar 

  28. Meyer, B.S., Matschiner, M., and Salzburger, W., A tribal level phylogeny of Lake Tanganyika cichlid fishes based on a genomic multi-marker approach, Mol. Phylogenet. Evol., 2015, vol. 83, pp. 56–71.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Musilová, Z., Schindler, I., and Staec, W., Description of Andinoacara stalsbergi sp. n. (Teleostei: Cichlidae: Cichlasomatini) from Pacific coastal rivers in Peru, and annotations on the phylogeny of the genus, Vertebr. Zool., 2009, vol. 59, pp. 131–141.

    Google Scholar 

  30. Musilová, Z., Říčan, O., Říčanová, Š., Janšta, P., Gahura, O., and Novák, J., Phylogeny and historical biogeography of trans-Andean cichlid fishes (Teleostei: Cichlidae), Vertebr. Zool., 2015, vol. 65, pp. 333–350.

    Google Scholar 

  31. Le Pabic, P., Cooper, W.J., and Schilling, T.F., Developmental basis of phenotypic integration in two Lake Malawi cichlids, EvoDevo, 2016, vol. 7, p. 3.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Parsons, K.J., Taylor, A.T., Powder, K.E., and Albertson, R.C., Wnt signalling underlies the evolution of new phenotypes and craniofacial variability in Lake Malawi cichlids, Nat. Comm., 2014, vol. 5, p. 3629.

    Article  CAS  Google Scholar 

  33. Piálek, L., Říčan, O., Casciotta, J., Almirón, A., and Zrzavý, J., Multilocus phylogeny of Crenicichla (Teleostei: Cichlidae), with biogeography of the C. lacustris group: species flocks as a model for sympatric speciation in rivers, Mol. Phylogenet. Evol., 2012, vol. 62, pp. 46–61.

    Article  PubMed  Google Scholar 

  34. Powder, K.E., Milch, K., Asselin, G., and Albertson, R.C., Constraint and diversification of developmental trajectories in cichlid facial morphologies, EvoDevo, 2015, vol. 6, p. 25.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Power, D.M., Llewellyn, L., Faustino, M., Björnsson, B.T., Einarsdottir, I.E., MCanario, A.V., and Sweeney, G.E., Thyroid hormones in growth and development of fish, Comp. Biochem. Physiol. Pt C: Toxicol. Pharmacol., 2001, vol. 130, pp. 447–459.

    CAS  Google Scholar 

  36. Prazdnikov, D.V. and Shkil, F.N., Effects of hyperthyroidism on the Labeobarbus (=Barbus) intermedius (Cyprinidae) early larval melanophores development, J. Ichthyol., 2016, vol. 56, pp. 321–324.

    Article  Google Scholar 

  37. Prazdnikov, D.V. and Shkil, F.N., Experimental evidence of the role of heterochrony in evolution of the Mesoamerican cichlids pigment patterns, Evol. Dev., 2019, vol. 21, pp. 3–15.

    Article  PubMed  Google Scholar 

  38. O’Quin, K.E., Smith, A.R., Sharma, A., and Carleton, K.L., New evidence for the role of heterochrony in the repeated evolution of cichlid opsin expression, Evol. Dev., 2011, vol. 13, pp. 193–203.

    Article  PubMed  Google Scholar 

  39. Rastorguev, S.M., Nedoluzhko, A.V., Levina, M.A., Prokhorchuk, E.B., Skryabin, K.G., and Levin, B.A., Pleiotropic effect of thyroid hormones on gene expression in fish as exemplified from the blue bream Ballerus ballerus (Cyprinidae): Results of transcriptomic analysis, Dokl. Biochem. Biophys., 2016, vol. 467, pp. 124–127.

    Article  CAS  PubMed  Google Scholar 

  40. Říčan, O., Musilová, Z., Muška, M., and Novák, J., Development of Coloration Patterns in Neotropical cichlids (Teleostei: Cichlidae: Cichlosomatinae), Brno: Folia Zoologica, 2005.

    Google Scholar 

  41. Říčan, O., Piálek, L., Dragová, K., and Novák, J., Diversity and evolution of the Middle American cichlid nfishes (Teleostei: Cichlidae) with revised classification, Vertebr. Zool., 2016, vol. 66, pp. 1–102.

    Google Scholar 

  42. Sabet, A. and Yen, P.M., Thyroid hormone action, in Clinical Management of Thyroid Disease, Wondisford, F.E. and Radovick, S., Eds., Philadelphia: Elsevier, 2009, pp. 43–56.

    Google Scholar 

  43. Salzburger, W., The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes, Mol. Ecol., 2009, vol. 18, pp. 169–185.

    Article  PubMed  Google Scholar 

  44. Schwarzer, J., Lamboj, A., Langen, K., Misof, B., and Schliewen, U.K., Phylogeny and age of chromidotilapiine cichlids (Teleostei: Cichlidae), Hydrobiologia, 2015, vol. 748, pp. 185–199.

    Article  CAS  Google Scholar 

  45. Shkil, F.N., Kapitanova, D.V., Borisov, V.B., Abdissa, B., and Smirnov, S.V., Thyroid hormone in skeletal development of cyprinids: effects and morphological consequences, J. Appl. Ichthyol., 2012, vol. 28, pp. 398–405.

    Article  CAS  Google Scholar 

  46. Viguerie, N. and Langin, D., Effect of thyroid hormone on gene expression, Curr. Opinion Clin. Nutrition Metab. Care, 2003, vol. 6, pp. 377–381.

    CAS  Google Scholar 

  47. Wijkmark, N., Kullander, S.O., and Barriga Salazar, R.E., Andinoacara blombergi, a new species from the río Esmeraldas basin in Ecuador and a review of A. rivulatus (Teleostei: Cichlidae). Explor. Freshwaters, 2012, vol. 23, pp. 117–137.

    Google Scholar 

  48. Yoo, J.H., Takeuchi, T., Tagawa, M., and Seikai, T., Effect of thyroid hormones on the stage-specific pigmentation of the Japanese flounder Paralichthys olivaceus, Zool. Sci., 2000, vol. 17, pp. 1101–1106.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071, Moscow, Russia

    D. V. Prazdnikov & F. N. Shkil

  2. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, 119334, Moscow, Russia

    F. N. Shkil

Authors
  1. D. V. Prazdnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. N. Shkil
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. V. Prazdnikov.

Additional information

The article was translated by the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prazdnikov, D.V., Shkil, F.N. The Experimental Heterochronies in a Green Terror Cichlid Andinoacara rivulatus (Teleostei: Cichlidae: Cichlasomatinae) Indicate a Role of Developmental Changes in the Cichlids Coloration Evolution. Biol Bull Russ Acad Sci 46, 56–64 (2019). https://doi.org/10.1134/S1062359019010102

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359019010102

Search

Navigation