Skip to main content
Log in

Ontogenetic mechanisms of explosive morphological divergence in the Lake Tana (Ethiopia) species flock of large African barbs (Labeobarbus; Cyprinidae; Teleostei)

  • Ontogeny and Evolution
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

Species flock of Lake Tana (Ethiopia) large African barbs (Labeobarbus; Cyprinidae; Teleostei), the largest recent cyprinid species flock, was studied as a model system for investigating ontogenetic mechanisms of the explosive morphological divergence often accompanying sympatric speciation in bony fishes. Comparative morphological analysis carried out with the use of geometric morphometric techniques revealed quantitative differences in the head shapes of species under study. Comparative analysis of skull development revealed significant interspecies differences in the temporal characteristics of craniogenesis in these species. These two lines of evidence suggest that heterochronies in craniogenesis underlie divergence in the head shapes of adult Tana barbs. This prediction was verified via experimental changes of temporal characteristics of craniogenesis in L. intermedius, a putative ancestor for the Lake Tana species flock. For this aim, timing and rate of skull development were changed by artificial manipulation of thyroid hormone levels. This experiment verified, that it is heterochronies that underlie an explosive morphological divergence of the Lake Tana barbs species flock. Our findings together with those reported in the literature suggest variability in the activity of the hypothalamic-pituitary-thyroid axis to contribute to these heterochronies.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alberch, P. and Alberch, J., Heterochronic mechanisms of morphological diversification and evolutionary change in the neotropical salamander, Bolitoglossa occidentalis (Amphibia: Plethodontidae), J. Morphol., 1981, vol. 167, pp. 249–264.

    Article  Google Scholar 

  • Albertson, R.C., Streelman, J.T., Kocher, T.D., et al., Integration and evolution of the cichlid mandible: molecular basis of alternate feeding strategies, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 16287–16292.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alekseev, S.S., Formation of morphological differences between the narrow-nosed and snub-nosed lenoks (genus Brachymystax, Salmonidae) in the ontogeny and the role of heterochrony in their divergence, Vopr. Ikhtiol., 1994, vol. 34, pp. 1–16.

    Google Scholar 

  • De Beer, G., Embryos and Ancestors, Oxford: Clarendon Press, 1940.

    Google Scholar 

  • Berrebi, P. and Valiushok, D., Genetic divergence among morphotypes of Lake Tana (Ethiopia) barbs, Biol. J. Linn. Soc., 1998, vol. 64, pp. 369–384.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bookstein, F., Morphometric Tools for Landmark Data: Geometry and Biology, Cambridge (UK): Cambridge Univ. Press, 1991.

    Google Scholar 

  • Borisov, V.B., Shkil, F.N., Abdissa, B., et al., Development of the cranium in the large African hexaploid barb Labeobarbus (=Barbus) intermedius (Cyprinidae; Teleostei), J. Ichthyol., 2012, vol. 52, no. 11, pp. 838–860.

    Article  Google Scholar 

  • Brown, D.D., The role of thyroid hormone in zebrafish and axolotl development, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 13011–13016.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Colosimo, P.F., Hosemann, K.E., Balabhadra, S., et al., Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles, Science, 2005, vol. 307, pp. 1928–1933.

    Article  CAS  PubMed  Google Scholar 

  • Durmowicz, M.C., Cui, C.Y., and Schlessinger, D., The EDA gene is target of, but does not regulate Wnt-signaling, Gene, 2002, vol. 285, pp. 203–211.

    Article  CAS  PubMed  Google Scholar 

  • Dzerzhinskii, K.F., Shkil, F.N., Belai Abdissa, et al., Spawning of large Barbus (Barbus intermedins complex) in a small river of the Lake Tana basin (Ethiopia) and relationships of some putative species, J. Ichthyol., 2007, vol. 47, no. 8, pp. 639–646.

    Article  Google Scholar 

  • Einarsdottir, I.E., Silva, N., Power, D.M., et al., Thyroid and pituitary gland development from hatching through metamorphosis of a teleost flatfish, the Atlantic halibut, Anat. Embryol., 2006, vol. 211, pp. 47–60.

    Article  PubMed  Google Scholar 

  • Golubtsov, A.S., Fish species flocks in lakes and rivers: sympatric divergence in faunistically depauperated fish communities as particular mode of evolution, in Current Topics Modern Ichthyology (The 100th Anniversary of G.V. Nikolsky), Pavlov, D.S., Dgebuadze, Yu., and Shatunovskii, M.I., Eds., Moscow: KMK, Scientific press, 2010, pp. 96–123.

    Google Scholar 

  • Gould, S.J., Ontogeny and Phylogeny, Cambridge: Harvard Univ. Press, 1977.

    Google Scholar 

  • de Graaf, M., Eshete Dejen., Osse, J.W.M., et al., Adaptive radiation of Lake Tana’s (Ethiopia) Labeobarbus species flock (Pisces, Cyprinidae), Mar. Freshwater Res., 2008, vol. 59, pp. 391–407.

    Article  Google Scholar 

  • de Graaf, M., Megens, H.-J., Samallo, J., et al., Preliminary insight into the age and origin of the Labeobarbus fish species flock from Lake Tana (Ethiopia) using the mtDNA cytochrome b gene, Mol. Phylogen. Evol., 2010, vol. 54, pp. 336–343.

    Article  Google Scholar 

  • Gunz, P. and Mitteroecker, P., Semilandmarks: a method for quantifying curves and surfaces, Hystrix, 2013, vol. 24, no. 1, pp. 103–109.

    Google Scholar 

  • Harada, Y., Harada, S., Kinoshita, I., et al., Thyroid gland development in a neotenic goby (ice goby, Leucopsarion petersii) and a common goby (ukigori, Gymnogobius urotaenia) during early life stages, Zool. Sci., 2003, vol. 20, no. 7, pp. 883–888.

    Article  PubMed  Google Scholar 

  • Hseu, J.-R., Chang, H.-F., and Ting, Y.-Y., Inducing effects of hormones in metamorphosis-arrested grouper larvae, J. Fish. Soc. Taiwan, 2002, vol. 29, pp. 79–83.

    CAS  Google Scholar 

  • Ishizuya-Oka, A., Hasebe, T., Shimizu, K., et al., Shh/BMP-4 signaling pathway is essential for intestinal epithelial development during Xenopus larval-to-adult remodeling, Dev. Dyn., 2006, vol. 235, pp. 3240–3249.

    Article  CAS  PubMed  Google Scholar 

  • Janz, D.M., Endocrine system, in The Laboratory Fish, Ostrander, G.K., Ed., London: Academic Press, 2000, pp. 189–217.

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

    Article  PubMed  Google Scholar 

  • de Jong, I.M.L., Colbert, M.W., Witte, F., et al., Polymorphism in developmental timing: intraspecific heterochrony in a Lake Victoria cichlid, Evol. Dev., 2009, vol. 11, pp. 625–635.

    Article  PubMed  Google Scholar 

  • Kitano, J., Lema, S.C., Luckenbach, J.A., et al., Adaptive divergence in the thyroid hormone signaling pathway in the stickleback radiation, Curr. Biol., 2010, vol. 20, no. 23, pp. 2124–2130.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Klingenberg, C.P., Evolution and development of shape: integrating quantitative approaches, Nature Rev., 2010, vol. 11, pp. 623–635.

    CAS  Google Scholar 

  • Kontula, T., Kirilchik, S.V., and Vainola, R., Endemic diversification of the monophyletic cottoid fish species flock in Lake Baikal explored with mtDNA sequencing, Mol. Phylogenet. Evol., 2003, vol. 27, pp. 143–155.

    Article  CAS  PubMed  Google Scholar 

  • Lassova, L., Niu, Z., Golden, E.B., et al., Thyroid hormone treatment of cultured chondrocytes mimics in vivo stimulation of collagen X mRNA by increasing BMP 4 expression, J. Cell Physiol., 2009, vol. 219, pp. 595–605.

    Article  CAS  PubMed  Google Scholar 

  • Loh, Y.H., Katz, L.S., Mims, M.C., Kocher, T.D., Yi, S.V., Streelman, J.T. Comparative analysis reveals signatures of differentiation amid genomic polymorphism in Lake Malawi cichlids. Genome Biol. 2008; 9(7): R113. doi: 10.1186/gb-2008-9-7-r113

    Article  PubMed Central  PubMed  Google Scholar 

  • McNamara, K.J., Heterochrony: the evolution of development, Evo. Edu. Outreach, 2012, vol. 5, pp. 203–218.

    Article  Google Scholar 

  • Meyer, A., Cichlid species flocks of the past and present, Heredity, 2005, vol. 95, pp. 419–420.

    Article  CAS  PubMed  Google Scholar 

  • Miller, L.D., Park, K.S., Guo, Q.M., et al., Silencing of Wnt signaling and activation of multiple metabolic pathways in response to thyroid hormone-stimulated cell proliferation, Mol. Cell Biol., 2001, vol. 21, pp. 6626–6639.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mina, M.V., Mironovsky, A.N., and Golani, D., Consequences and modes of morphological diversification of East African and Eurasian barbins (genera Barbus, Varicorhinus and Capoeta) with particular reference to Barbus intermedius complex, Env. Biol. Fish, 2001, vol. 61, pp. 241–252.

    Article  Google Scholar 

  • Mina, M.V., Mironovsky, A.N., and Kapitanova, D.V., Phenetic relationships and probable ways of morphological diversification of the African large barbs (Barbus intermedius complex) in Lake Tana (Ethiopia), J. Ichthyol., 2011, vol. 51, no. 2, pp. 137–151.

    Article  Google Scholar 

  • Mitteroecker, P. and Gunz, P., Advances in geometric morphometrics, Evol. Biol., 2009, vol. 36, pp. 235–247.

    Article  Google Scholar 

  • Mulholland, D., Dedhar, S., Coetzee, G., et al., Interaction of nuclear receptors with the Wnt/ß-catenin/Tcf signaling axis: Wnt—you like to know?, Endocr. Rev., 2005, vol. 26, no. 7, pp. 898–915.

    Article  CAS  PubMed  Google Scholar 

  • Nagelkerke, L.A.J. and Sibbing, F.A., The ‘Barbus’ intermedius species flock of Lake Tana (Ethiopia). I. The ecological and evolutionary significance of morphological diversity, Ital. J. Zool., 1998, vol. 65, pp. 3–7.

    Article  Google Scholar 

  • Nagelkerke, L.A.J. and Sibbing, F.A., The large barbs (Barbus spp., Cyprinidae, Teleostei) of Lake Tana (Ethiopia), with a description of a new species, Barbus osseensis, Netherl. J. Zool., 2000, vol. 50, pp. 179–214.

    Article  Google Scholar 

  • Okada, N., Morita, T., Tanaka, M., et al., Thyroid hormone deficiency in abnormal larvae of the Japanese flounder Paralichthys olivaceus, Fish. Sci., 2005, vol. 71, pp. 107–114.

    Article  CAS  Google Scholar 

  • Osinov, A.G., Arctic charr Salvelinus alpinus from Transbaikalia and Taimyr: genetic differentiation and origin, J. Ichthyol., 2002, vol. 42, no. 2, pp. 141–151.

    Google Scholar 

  • Parsons, K.J. and Albertson, R.C., Roles for Bmp4 and CaM1 in shaping the jaw: evo-devo and beyond, Ann. Rev. Genet., 2009, vol. 43, pp. 369–388.

    Article  CAS  PubMed  Google Scholar 

  • Parsons, K.J., Taylor, A.T., Powder, K.E., et al., Wnt signalling underlies the evolution of new phenotypes and craniofacial variability in Lake Malawi cichlids, Nature Commun., 2014, vol. 5, p. 3629. DOI: 10.1038/ncomms4629

    Article  Google Scholar 

  • Pavlinov, I.Ya. and Mikeshina, N.G., Principles and methods of geometric morphometry, Zh. Obshch. Biol., 2002, vol. 63, no. 6, pp. 473–493.

    PubMed  Google Scholar 

  • Pichugin, M.Yu., Development of skeleton elements in juvenile dwarf and small sympatric forms of Salvelinus alpinus complex from Lake Davatchan (Transbaikalia), J. Ichthyol., 2009, vol. 49, no. 9, pp. 741–758.

    Article  Google Scholar 

  • Raff, R.A. and Kaufman, T.C., Embryos, Genes, and Evolution: The Developmental-Genetic Basis of Evolutionary Change, Macmillan, 1983.

    Google Scholar 

  • Reig, S., Doadrio, I., and Mironovsky, A.N., Geometric analysis of size and shape variation in barbel from Lake Tana (Ethiopia), Folia Zool., 1998, vol. 47, suppl. 1, pp. 35–51.

    Google Scholar 

  • Ribbink A.J., Is the species flock concept tenable?, in Evolution of Fish Species Flocks, Echelle, A.A. and Kornfield, I., Eds., Univ. Maine: Orono Press, 1984, pp. 21–25.

    Google Scholar 

  • Salzburger, W., Meyer, A., Baric, S., et al., Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas, Syst. Biol., 2002, vol. 51, no. 1, pp. 113–135.

    Article  PubMed  Google Scholar 

  • Shkil, F.N., Borisov, V.B., Abdissa, B., et al., Role of thyroid hormone in the ontogeny and morphological diversification of Barbus intermedius sensu Banister, 1973 of Lake Tana in Ethiopia, Russ. J. Dev. Biol., 2010, vol. 41, no. 6, pp. 369–380.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schmalhausen, I.I., Organizm kak tseloe v individual’nom i istoricheskom razvitii (The Organism as a Whole in Individual and Historical Development), Moscow: Izd. AN SSSR, 1938.

    Google Scholar 

  • Sibbing, F.A., Nagelkerke, L.A.J., Stet, R.J.M., et al., Speciation of endemic Lake Tana barbs (Cyprinidae, Ethiopia) driven by trophic resource partitioning; a molecular and ecomorphological approach, Aquat. Ecol., 1998, vol. 32, pp. 217–227.

    Article  Google Scholar 

  • Sideleva, V.G., The Patterns of lake speciation and the coupled morphological and molecular divergence of endemic fish of Lake Baikal, in Current Topics of Modern Ichthyology (The 100th Anniversary of G.V. Nikolsky), Pavlov, D.S., Dgebuadze, Yu.Yu., and Shatunovskii, M.I., Eds., Moscow: KMK, Scientific Press, 2010,pp. 124–147.

    Google Scholar 

  • Sideleva, V.G., Speciation of endemic Cottoidei in Lake Baikal, Adv. Limnol., 1994, vol. 44, pp. 441–450.

    Google Scholar 

  • Skulason, S., Noakes, D.L.G., and Snorrason, S.S., Ontogeny of trophic morphology in four sympatric morphs of arctic charr Salvelinus alpinus in Thingvallavatn, Iceland, Biol. J. Linn. Soc., 1989, vol. 38, pp. 281–301.

    Article  Google Scholar 

  • Smirnov, S.V., Kapitanova, D.V., Borisov, V.B., et al., Lake Tana large barbs diversity: developmental and hormonal bases, J. Ichthyol., 2012, vol. 52, no. 11, pp. 861–880.

    Article  Google Scholar 

  • Sullivan, J.P., Lavoue, S., and Hopkins, C.D., Discovery and phylogenetic analysis of a riverine species flock of African electric fishes (Mormyridae: Teleostei), Evolution, 2002, vol. 56, no. 3, pp. 597–616.

    Article  CAS  PubMed  Google Scholar 

  • Turgeon, J., Estoup, A., and Bernatchez, L., Species flock in the North American lakes: molecular ecology of Lake Nipigon ciscoes (Teleostei: Coregonidae: Coregonus), Evolution, 1999, vol. 53, pp. 1857–1871.

    Article  CAS  Google Scholar 

  • Walker, M.B. and Kimmel, C.B., A two-color acid-free cartilage and bone stain for zebrafish larvae, Biotech. Histochem., 2007, vol. 82, pp. 23–28.

    Article  CAS  PubMed  Google Scholar 

  • Wang, L., Shao, Y.Y., and Ballock, R.T., Thyroid hormone interacts with the Wnt/ß-catenin signaling pathway in the terminal differentiation of growth plate chondrocytes, J. Bone Mineral Res., 2007, vol. 22, no. 12, pp. 1988–1995.

    Article  CAS  Google Scholar 

  • West-Eberhard, M.J., Developmental plasticity and evolution, Oxford: Oxford Univ. Press, 2003.

    Google Scholar 

  • Yablokov, A.V. and Yusufov, A.G., Evolyutsionnoe uchenie. Ucheb. posobie dlya studentov un-tov (Evolutionary Theory: A Manual for High School Students), Moscow: Vysshaya shkola, 1976.

    Google Scholar 

  • Yamano, K., Tagawa, M., de Jesus, E.G., et al., Changes in whole body concentrations of thyroid hormones and cortisol in metamorphosing conger eel, J. Comp. Physiol., 1991, vol. 161, no. 4, pp. 371–375.

    Article  CAS  Google Scholar 

  • Zelditch, M.L., Lundrigan, B.L., and Garland, T., Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance, Evol. Dev., 2004, vol. 6, pp. 194–206.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. N. Shkil.

Additional information

Original Russian Text © F.N. Shkil, O.E. Lazebnyi, D.V. Kapitanova, Belay Abdissa, V.B. Borisov, S.V. Smirnov, 2015, published in Ontogenez, 2015, Vol. 46, No. 5, pp. 346–359.

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

Shkil, F.N., Lazebnyi, O.E., Kapitanova, D.V. et al. Ontogenetic mechanisms of explosive morphological divergence in the Lake Tana (Ethiopia) species flock of large African barbs (Labeobarbus; Cyprinidae; Teleostei). Russ J Dev Biol 46, 294–306 (2015). https://doi.org/10.1134/S1062360415050069

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360415050069

Keywords

Navigation