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Intra- and interspecific variability of the cranial ossification sequences in Barbus sensu lato.

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Abstract

Analysis of the developmental sequence variability provides data linking the ontogeny and phylogeny of the investigated objects. Here, we present a study of cranial ossifications sequence variability in the polyphyletic group of Cyprininae Barbus sensu lato (Cypriniformes, Teleostei). We analyzed the intra- and interspecific variability, compared sequences of closely related and phylogenetically distant species, reconstructed an alleged ancestral sequence, and assessed the sequence variations’ evolutionary validity. As the results, we revealed that the observed sequence alterations occur due to intrinsic, likely genetic or epigenetic factors. The skull ossifications, as well as skull regions, differ in the variability level. The ossifications appearing at the intermediate phase and skull regions composing splanchnocranium are most variable. In contrast, the structures emerging at the early and late phases of skull development and regions of neurocranium are less variable. The majority of sequence alterations are non-adaptive and selectively neutral. Increase in their number accompanying the transition from intra- to interspecific and intergeneric levels resembles the accumulation of the selectively neutral genetic variations accompanying the increase of phylogenetic distance. Reconstructions of phylogenetic relationships between investigated species obtained with the analyses of sequence similarity and phylogenetic analyses using parsimony (PAUP) are consistent with the phylogenies based on molecular data and thus demonstrate the potential of sequence analysis for phylogenetic inference.

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Data Availability

All data generated or analyzed during this study are included in this published article.

Abbreviations

AS:

Ancestral sequence

COS:

Complete ossification sequence

dpf:

Days post fertilization

MCS:

Most common sequence

mMRD:

Mean magnitude of rank differences

MRD:

Magnitude of rank differences

P10% :

10th percentile

P90% :

90th percentile

SD:

Standard deviation

SE:

Standard error

SL:

Standard length

References

  • Aguirre, C. L., Hand, S. J., Koyabu, D., Son, N. T., & Wilson, L. A. B. (2019). Postcranial heterochrony, modularity, integration and disparity in the prenatal ossification in bats (Chiroptera). BMC Evolutionary Biology, 19(1), 75.

    Article  Google Scholar 

  • Alekseyev, S. S., Dgebuadze, Y. Y., Mina, M. V., & Mironovsky, A. N. (1996). Small ‘Large Barbs’ spawning in tributaries of Lake Tana: what are they. Folia Zoologica, 45(S1), 85–96.

    Google Scholar 

  • Berrebi, P., Chenuil, A., Kotlik, P., Machordom, A., & Tsigenopoulos, C. S. (2014). Disentangling the evolutionary history of the genus Barbus sensu lato, a twenty years adventure. In M. J. Alves, A. Cartaxana, A. M. Correia, & L. F. Lopes (Eds.), Professor Carlos Almaça (1934–2010)—Estado da Arte em Áreas Cientifi cas que Desenvolveu (pp. 29–55). Museu Nacional de História Natural e da Ciéncia.

    Google Scholar 

  • Berrebi, P., Kottelat, M., Skelton, P., & Rab, P. (1996). Systematics of barbus: State of the art and heuristic comments. Folia Zoologica, 45(Suppl. 1), 5–12.

    Google Scholar 

  • Beshera, K. A., & Harris, P. M. (2014). Mitochondrial DNA phylogeography of the Labeobarbus intermedius complex (Pisces, Cyprinidae) from Ethiopia. Journal of Fish Biology, 85, 228–245.

    Article  CAS  PubMed  Google Scholar 

  • Block, A. J., & Mabee, P. M. (2012). Development of the mandibular, hyoid arch and gill arch skeleton in the Chinese barb Puntius semifasciolatus: Comparisons of ossification sequences among Cypriniformes. Journal of Fish Biology, 81, 54–80.

    Article  CAS  PubMed  Google Scholar 

  • Borisov, V. B., Shkil, F. N., Abdissa, B., & Smirnov, S. V. (2012). Development of the Cranium in the Large African Hexaploid Barb Labeobarbus (=Barbus) intermedius (Cyprinidae; Teleostei). J. Ichthiol, 52(11), 838–860.

    Article  Google Scholar 

  • Britz, R., & Conway, K. (2011). The Cypriniformes Tree of Confusion. Zootaxa, 2946, 73–78.

    Article  Google Scholar 

  • Chang, C. T., & Franz-Odendaal, T. A. (2014). Perturbing the developing skull: Using laser ablation to investigate the robustness of the infraorbital bones in zebrafish (Danio rerio). BMC Developmental Biology, 14, 44.

    Article  PubMed  PubMed Central  Google Scholar 

  • Coe, T. S., Hamilton, P. B., Griffiths, A. M., Hodgson, D. J., Wahab, N. A., & Tyler, C. R. (2009). Genetic variations in strains of zebrafish (Danio rerio) and the implications for ecotoxicology studies. Ecotoxicology, 18, 144–150.

    Article  CAS  PubMed  Google Scholar 

  • Colbert, M. W., & Rowe, T. (2008). Ontogenetic Sequence Analysis: Using parsimony to characterize developmental sequences and sequence polymorphism. Journal of Experimental Zoology. Part b, Molecular and Developmental Evolution, 310(5), 398–416.

    Article  PubMed  Google Scholar 

  • Conway, K.W. & Moritz, T. (2006). Barboides britzi, a new species of miniature cyprinid from Benin (Ostariophysi: Cyprinidae), with a neotype designation for B. gracilis. Ichthyol Explor Freshwaters, 17(1), 73–84.

  • Cubbage, C. C., & Mabee, P. M. (1996). Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi; Cyprinidae). Journal of Morphology, 229, 121–160.

    Article  PubMed  Google Scholar 

  • Day, S. W., Higham, T. E., Holzman, R., & Wassenbergh, S. V. (2015). Morphology, kinematics, and dynamics: The mechanics of suction feeding in fishes. Integrative and Comparative Biology, 55(1), 21–35.

    Article  PubMed  Google Scholar 

  • De Graaf, M., Dejen, E., Osse, J. W. M., & Sibbing, F. A. (2008). Adaptive radiation of Lake Tana’s (Ethiopia) Labeobarbus species flock (Pisces, Cyprinidae). Marine and Freshwater Research, 59, 391–407.

    Article  Google Scholar 

  • De Graaf, M., Megens, H. J., & Samallo, J. (2010). Preliminary insight into the age and origin of the Labeobarbus fish species flock from Lake Tana (Ethiopia) using mtDNA cytochrome b gene. Molecular Phylogenetics and Evolution, 54, 336–343.

    Article  PubMed  Google Scholar 

  • De Jong, I. M. L., Witte, F., & Richardson, M. K. (2009). Developmental stages until hatching of the Lake Victoria cichlid Haplochromis piceatus. Journal of Morphology, 270, 519–535.

    Article  PubMed  Google Scholar 

  • Dejen, E., Rutjes, H. A., de Graaf, M., Nagelkerke, L. A. G., Osse, J. W. M., & Sibbing, F. A. (2002). The ‘small barbs’ Barbus humilis and B. trispilopleura of Lake Tana (Ethiopia): Are they ecotypes of the same species? Environmental Biology of Fishes, 65, 373–386.

    Article  Google Scholar 

  • Dzerzhinskii, K. F., Shkil, F. N., Abdissa, B., Zelalem, W., & Mina, M. V. (2007). Spawning of large Barbus (Barbus intermedins Complex) in a small river of the Lake Tana basin (Ethiopia) and relationships of some putative species. Journal of Ichthyology, 47, 639–646.

    Article  Google Scholar 

  • Faustino, M., & Power, D. M. (2001). Osteologic development of the viscerocranial skeleton in sea bream: Alternative ossification strategies in teleost fish. Journal of Fish Biology, 58, 537–572.

    Article  Google Scholar 

  • Grosso, J., Baldo, D., Costa, C. S., Natale, G. S., & Candiote, F. V. (2019). Embryonic ontogeny of three species of Horned Frogs, with a review of early development in Ceratophryidae. Journal of Morphology, 281, 17–32.

    Article  PubMed  Google Scholar 

  • Harrington, S. M., Harrison, L. B., & Sheil, C. A. (2013). Ossification sequence heterochrony among amphibians. Evolution & Development, 15, 344–364.

    Article  CAS  Google Scholar 

  • Hayes, M. M., & Armbruster, J. W. (2017). The taxonomy and relationships of the African small barbs (Cypriniformes: Cyprinidae). Copeia, 105(2), 348–362.

    Article  Google Scholar 

  • Herre, A. W. C. T. (1933). The fishes of Lake Lanao: A problem in evolution. The American Naturalist, 67(709), 154–162.

    Article  Google Scholar 

  • Jeffery, J. E., Richardson, M. K., Coates, M. I., & Bininda-Emonds, O. R. P. (2002). Analyzing developmental sequences within a phylogenetic framework. Syst. Bio., 51, 478–491.

    Article  Google Scholar 

  • Keyte, A. L., & Smith, K. K. (2014). Heterochrony and developmental timing mechanisms: Changing ontogenies in evolution. Seminars in Cell & Developmental Biology, 34, 99–107.

    Article  Google Scholar 

  • Koyabu, D., & Son, N. T. (2014). Patterns of postcranial ossification and sequence heterochrony in bats: Life histories and developmental trade-offs. Journal of Experimental Zoology. Part b, Molecular and Developmental Evolution, 322(8), 607–618.

    Article  PubMed  Google Scholar 

  • Levin, B. A., Casal-López, M., Simonov, E., Dgebuadze, Y. Y., Mugue, N. S., Tiunov, A. V., Doadrio, I., & Golubtsov, A. S. (2019). Adaptive radiation of barbs of the genus Labeobarbus (Cyprinidae) in an East African river. Freshwater Biology, 64, 1721–1736.

    Article  CAS  Google Scholar 

  • Levin, B. A., Freyhof, J., Lajbner, Z., Perea, S., Abdoli, A., Gaffaroğlu, M., Özuluğ, M., Rubenyan, H. R., Salnikov, V. B., & Doadrio, I. (2012). Phylogenetic relationships of the algae scraping cyprinid genus Capoeta (Teleostei: Cyprinidae). Molecular Phylogenetics and Evolution, 62(1), 542–549.

    Article  PubMed  Google Scholar 

  • Li, X., & Guo, B. (2020). Substantially adaptive potential in polyploid cyprinid fishes: Evidence from biogeographic, phylogenetic and genomic studies. Proceedings of the Royal Society B, 287(20193008), 20193008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mabee, P. M., Olmstead, K. L., & Cubbage, C. C. (2000). An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution, 54(6), 2091–2106.

    Article  CAS  PubMed  Google Scholar 

  • Mabee, P. M., & Trendler, T. A. (1996). Development of the cranium and paired fins in Betta splendens (Teleostei: Percomorpha): Intraspecific variation and interspecific comparisons. Journal of Morphology, 227, 249–287.

    Article  PubMed  Google Scholar 

  • Machordom, A., & Doadrio, I. (2001). Evolutionary history and speciation modes in the cyprinid genus Barbus. Proceedings of the Royal Society of London. B. Biological Sciences, 268, 1297–1306.

    Article  CAS  Google Scholar 

  • Maxwell, E. E., & Harrison, L. B. (2009). Methods for the analysis of developmental sequence data. Evolution & Development, 11, 109–119.

    Article  CAS  Google Scholar 

  • McNamara, K. J. (2012). Heterochrony: The evolution of development. Evolution: Education and Outreach, 5, 203–218.

    Google Scholar 

  • Mitgutsch, C., Wimmer, C., Sanchez-Villagra, M. R., Hahnloser, R., & Schneider, R. A. (2011). Timing of ossification in duck, quail, and zebra finch: Intraspecific variation, heterochronies, and life history evolution. Zoological Science, 28(7), 491–500.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagelkerke, L. A. J., Leon-Kloosterziel, K. M., Megens, H.-J., De Graaf, M., Diekmann, O. E., & Sibbing, F. A. (2015). Shallow genetic divergence and species delineations in the endemic Labeobarbus species flock of Lake Tana, Ethiopia. Journal of Fish Biology, 87, 1191–1208.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Nagelkerke, L. J., & Sibbing, F. A. (2001). Resource partitioning by Lake Tana barbs predicted from fish morphometrics and prey characteristics. Reviews in Fish Biology and Fisheries, 10, 393–437.

    Google Scholar 

  • Pasco-Viel, E., Yang, L., Veran, M., Balter, V., Mayden, R. L., Laudet, V., & Viriot, L. (2014). Stability versus diversity of the dentition during evolutionary radiation in cyprinine fish. Proceedings of the Royal Society B, 281, 20132688.

    Article  PubMed  PubMed Central  Google Scholar 

  • Powers, A. K., Boggs, T. E., & Gross, J. B. (2018). Canal neuromast position prefigures developmental patterning of the suborbital bone series in Astyanax cave- and surface-dwelling fish. Developmental Biology, 441(2), 252–261.

    Article  CAS  PubMed  Google Scholar 

  • Ren, Q., & Mayden, R. L. (2016). Molecular phylogeny and biogeography of African diploid barbs, ‘Barbus’, and allies in Africa and Asia (Teleostei: Cypriniformes). Zoologica Scripta, 45(6), 642–649.

    Article  Google Scholar 

  • Samallo, J., Megens, H., De Graaf, M., & Sibbing, F. (2007). Evolutionary origin of Lake Tana’s (Ethiopia) small Barbus species: Indications of rapid ecological divergence and speciation. Animal Biology, 57(1), 39–48.

    Article  Google Scholar 

  • Schoch, R. R. (2006). Skull ontogeny: Developmental patterns of fishes conserved across major tetrapod clades. Evolution & Development, 8, 524–536.

    Article  Google Scholar 

  • Sheil, C. A., & Greenbaum, E. (2005). Reconsideration of skeletal development of Chelydra serpentina (Reptilia: Testudinata: Chelydridae): Evidence for intraspecific variation. Journal of Zoology, 265, 235–267.

    Article  Google Scholar 

  • Shkil, F. N., Dzerzhinskii, K. F., Abdissa, B., Borisov, V. B., Zelalem, W., Kapitanova, D. V., Tsegaw, M., & Smirnov, S. V. (2017). Notes on the breeding of large Lake Tana Barbs (Labeobarbus Spp.) in nature and laboratory. Ethiopian Journal of Biological Sciences, 16, 149–170.

    Google Scholar 

  • Smirnov, S. V., Borisov, V. B., Kapitanova, D. V., Abdissa, B., & Shkil, F. N. (2012). Heterochronies in skull development of Lake Tana large African barbs (Labeobarbus; Cyprinidae; Teleostei). Journal of Applied Ichthyology, 28, 406–410.

    Article  Google Scholar 

  • Smith, K. K. (2001). Heterochrony revisited: The evolution of developmental sequences. Bio J Linn Soc., 73, 169–186.

    Article  Google Scholar 

  • Spiekman, S., & Werneburg, I. (2017). Patterns in the bony skull development of marsupials: High variation in onset of ossification and conserved regions of bone contact. Science and Reports, 7, 43197.

    Article  CAS  Google Scholar 

  • Stout, C. C., Tan, M., Lemmon, A. R., Lemmon, E. M., & Armbruster, J. W. (2016). Resolving Cypriniformes relationships using an anchored enrichment approach. BMC Evolutionary Biology, 16, 244.

    Article  PubMed  PubMed Central  Google Scholar 

  • Strauss, R. E. (1990). Heterochronic variation in the developmental timing of cranial ossifications in poeciliid fishes (Cyprinodontiformes). Evolution, 44, 1558–1567.

    Article  PubMed  Google Scholar 

  • Swofford, D. L. (2002). PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sunderland, MA, USA: Sinauer Associates.

    Google Scholar 

  • Tills, O., Rundle, S. D., Salinger, M., Haun, T., Pfenninger, M., & Spicer, J. I. (2011). A genetic basis for intraspecific differences in developmental timing? Evolution & Development, 13(6), 542–548.

    Article  Google Scholar 

  • Tsigenopoulos, C. S., Rab, P., Naran, D., & Berrebi, P. (2002). Multiple origins of polyploidy in the phylogeny of Southern African barbs (Cuprinidae) as inferred from mtDNA markers. Heredity, 88, 466–473.

    Article  CAS  PubMed  Google Scholar 

  • Vandewalle, P., Focant, B., Huriaux, F., & Chardon, M. (1992). Early development of the cephalic skeleton of Barbus barbus (Teleostei, Cyprinidae). Journal of Fish Biology, 41, 43–62.

    Article  Google Scholar 

  • Vreven, E., Musschoot, T., Snoeks, J., & Schliewen, U. K. (2016). The African hexaploid Torini (Cypriniformes: Cyprinidae): Review of a tumultuous history. Zoological Journal of the Linnean Society, 177(2), 295.

    Article  Google Scholar 

  • Wake, D. B., Roth, G., & Wake, M. H. (1983). On the problem of stasis in organismal evolution. Journal of Theoretical Biology, 101(2), 211–224.

    Article  Google Scholar 

  • Walker, M. B., & Kimmel, C. B. (2007). A two-color acid-free carlilage and bone stain for zebrafish. Biotechnic and Histochemistry, 82, 23–28.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., Wu, X., Chen, Z., Yue, Z., Ma, W., Chen, S., Xiao, H., Murphy, R. W., Zhang, Y., Zan, R., & Luo, J. (2013). Molecular phylogeny of European and African Barbus and their West Asian relatives in the Cyprininae (Teleostei: Cypriniformes) and orogenesis of the Qinghai-Tibetan Plateau. Chinese Sci Bull, 58(31), 3738–3746.

    Article  CAS  Google Scholar 

  • Werneburg, I., & Sánchez-Villagra, M. R. (2015). Skeletal heterochrony is associated with the anatomical specializations of snakes among squamate reptiles. Evolution, 69, 254–263.

    Article  PubMed  Google Scholar 

  • Wilson, L. A. B., Schradin, C., Mitgutsch, C., Galliari, F. C., Mess, A., & Sánchez-Villagra, M. R. (2010). Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia). Organisms, Diversity and Evolution, 10, 243–258.

    Article  Google Scholar 

  • Wongyai, N., Jutagate, A., Grudpan, C., & Jutagate, T. (2020). Condition index, reproduction and feeding of three non-obligatory riverine Mekong cyprinids in different environments. Tropical Life Sciences Research, 31(2), 159–173.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, L., Naylor, G. J. P., & Mayden, R. L. (2022). Deciphering reticulate evolution of the largest group of polyploid vertebrates, the subfamily cyprininae (Teleostei: Cypriniformes). Mol Phylogenet Evol, 166, 107323.

    Article  PubMed  Google Scholar 

  • Yang, L., Sado, T., Hirt, M. V., Pasco-Viel, E., Arunachalam, M., Li, J., Wang, X., Freyhof, J., Saitoh, K., Simons, A. M., Miya, M., He, S., & Mayden, R. L. (2015). Phylogeny and polyploidy: Resolving the classification of cyprinine fishes (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution, 85, 97–116.

    Article  PubMed  Google Scholar 

  • Zheng, L.-P., Yang, J.-X., & Chen, X.-Y. (2016). Molecular phylogeny and systematics of the Barbinae (Teleostei: Cyprinidae) in China inferred from mitochondrial DNA sequences. Biochemical Systematics and Ecology, 68, 250–259.

    Article  CAS  Google Scholar 

  • Ziermann, J. M., Mitgutsch, C., & Olsson, L. (2014). Analyzing developmental sequences with Parsimov—A case study of cranial muscle development in anuran larvae. J Exp Zool Mol Dev Evol, 322B, 586–606.

    Article  Google Scholar 

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Acknowledgements

Authors are sincerely grateful to Joint Ethio-Russian biological expedition (JERBE) and Dr. A.A. Darkov, Bahir-Dar fishery and other aquatic life research center (BFALRC ARARI, Ethiopia), A.D. Fau (Riofrio 1936 S.L., Spain), Dr. E.G. Mishvelov and Dr. A.A. Tsessarsky for the comprehensive assistance and support of work. The study was partially conducted within the frame of the projects 17-04-01617 and 20-04-00655 of Russian Foundation for Basic Research, and IDB RAS Research program No. 0088-2021-0019.

Funding

The study was supported by the Russian Foundation for Basic Research, project nos. 17–04-01617 and 20–04-00655.

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Authors and Affiliations

  1. A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky pr., 33, 119071, Moscow, Russia

    Fedor N. Shkil, Vasily Borisov, Dmitry Seleznev, Daria Kapitanova, Kirill Dzerzhinskii & Sergei Smirnov

  2. N.K. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Vavilova str., 26, 119334, Moscow, Russia

    Fedor N. Shkil & Daria Kapitanova

  3. I.D. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742, Borok, Russia

    Dmitry Seleznev

  4. Bahir Dar Fisheries and Other Aquatic Life Research Center, P.O. Box 794, Bahir Dar, Ethiopia

    Belay Abdissa

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  1. Fedor N. Shkil
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  2. Vasily Borisov
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  3. Dmitry Seleznev
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  4. Daria Kapitanova
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  6. Kirill Dzerzhinskii
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Correspondence to Fedor N. Shkil.

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Shkil, F.N., Borisov, V., Seleznev, D. et al. Intra- and interspecific variability of the cranial ossification sequences in Barbus sensu lato.. Evol Biol 49, 189–204 (2022). https://doi.org/10.1007/s11692-022-09563-3

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