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Flexibility of life to survive limitations: oral disc forms in the Tashan Cave barb Garra tashanensis

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Abstract

In this study, we analyzed nuclear DNA (nDNA) variation by means of genotyping-by-sequencing (GBS) of three disc-bearing and seven non-disc-bearing Garra tashanensis from the Tashan Cave in Iran to clarify their systematic and ecological relationships. We performed genetic differentiation, NeighborNet, Admixture, and principal component analyses on genomic data. Admixture and principal component analyses revealed clear genetic differentiation between disc-bearing and non-disc-bearing morphotypes, which was not detected by mtDNA markers in previous work. However, there was a non-disc-bearing individual that clustered with disc-bearing individuals. Based on the results of this study, the most parsimonious justification for coexistence of disc-bearing and non-disc-bearing forms of Garra in Tashan Cave is a combination of mechanisms similar to character release (intra-specific morphological diversification to exploit a wider range of habitats in the absence of competitors or predators) and relaxed selection (no more selective advantage for a previously advantageous trait as a result of ecological changes). The detected genetic structure may be an indication of reproductive isolation between the two groups. These data imply that the respective forms of the Tashan Cave barb could be a case of ongoing sympatric speciation, but also that disc form cannot be used as a taxonomic character for Tashan Cave barb forms.

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Genomic data are available with request.

References

  • Abed A, Légaré G, Pomerleau S, St-Cyr J, Boyle B, Belzile FJ (2019) Genotyping-by-sequencing on the ion torrent platform in barley. In: Harwood W (ed) Barley. Methods in molecular biology, vol 1900. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-8944-7_15

    Chapter  Google Scholar 

  • Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19(9):1655–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25(22):4692–4693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell MA, Aguirre WE (2013) Contemporary evolution, allelic recycling, and adaptive radiation of the threespine stickleback. Evol Ecol Res 15(4):377–411

    Google Scholar 

  • Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S, Simakov O, Ng AY, Lim ZW, Bezault E, Turner-Maier J (2014) The genomic substrate for adaptive radiation in African cichlid fish. Nature 513(7518):375–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodersen J, Post DM, Seehausen O (2018) Upward adaptive radiation cascades: predator diversification induced by prey diversification. Tr Ecol Evol 33(1):59–70

    Article  Google Scholar 

  • Chaves JA, Cooper EA, Hendry AP, Podos J, De León LF, Raeymaekers JA, MacMillan WO, Uy JA (2016) Genomic variation at the tips of the adaptive radiation of Darwin’s finches. Mol Ecol 25(21):5282–5295

    Article  CAS  PubMed  Google Scholar 

  • Çicek E, Secer B, Özturk S, Sungur S (2021) Age and growth of Garra rufa (Heckel, 1843) from Merzimen Stream, Euphrates River basin, Turkey. J Limnol Freshwat Fish Res 7(1):77–82

    Article  Google Scholar 

  • De Silva K (1991) Population dynamics and production of the rocky stream-dwelling fish Garra ceylonensis (Cyprinidae) in Sri Lanka. J Trop Ecol 7(3):289–303

    Article  Google Scholar 

  • Esin EV, Markevich GN, Pichugin MY (2018) Juvenile divergence in adaptive traits among seven sympatric fish ecomorphs arises before moving to different lacustrine habitats. J Evol Biol 31(7):1018–1034

    Article  PubMed  Google Scholar 

  • Gordeeva NV, Alekseyev SS, Matveev AN, Samusenok VP (2015) Parallel evolutionary divergence in Arctic char Salvelinus alpinus complex from Transbaikalia: variation in differentiation degree and segregation of genetic diversity among sympatric forms. Can J Fish Aquat Sci 72(1):96–115

    Article  Google Scholar 

  • Hamidan N, Britton JR (2015) Age and growth rates of the critically endangered fish Garra ghorensis can inform their conservation management. Aquat Conserv Mar Freshwat Ecosyst 25(1):61–70

    Article  Google Scholar 

  • Hashemzadeh Segherloo I, Abdoli A, Eagderi S, Esmaeili HR, Sayyadzadeh G, Bernatchez L, Hallerman E, Geiger MF, Özulug M, Laroche J, Freyhof J (2017) Dressing down: convergent reduction of the mental disc in Garra (Teleostei: Cyprinidae) in the Middle East. Hydrobiologia 785:47–59

    Article  Google Scholar 

  • Hashemzadeh Segherloo I, Najafi Chaloshtory S, Naser MD, Yasser AG, Tabatabaei SN, Piette-Lauziere G, Mashtizadeh A, Elmi A, Sedighi O, Changizi A, Hallerman E (2022) Sympatric morphotypes of the restricted-range Tashan Cave Garra: distinct species or a case of phenotypic plasticity? Environ Biol Fish 105(9):1251–1260

    Article  Google Scholar 

  • Hashemzadeh Segherloo I, Normandeau E, Benestan L, Rougeux C, Coté G, Moore JS, Ghaedrahmati N, Abdoli A, Bernatchez L (2018) Genetic and morphological support for possible sympatric origin of fish from subterranean habitats. Sci Rep 8(1):2909

    Article  PubMed  PubMed Central  Google Scholar 

  • Hashemzadeh Segherloo I, Rahmati S, Purahmad R, Golzarianpour K, Abdoli A (2013) Analysis of the systematic status of the blind Iran cave barb, Iranocypris typhlops, using COI gene. Mod Genet 8(1):59–66 (in Persian with English abstract)

    Google Scholar 

  • Howarth FG, Moldovan OT (2018a) The ecological classification of cave animals and their adaptations. In: Moldovan O, Kováč Ľ, Halse S (eds) Cave ecology. Ecological Studies (vol. 235). Springer, Cham. https://doi.org/10.1007/978-3-319-98852-8_4

    Chapter  Google Scholar 

  • Howarth FG, Moldovan OT (2018b) Where cave animals live. In: Moldovan O, Kováč Ľ, Halse S (eds) Cave ecology. Ecological Studies, vol 235. Springer, Cham. https://doi.org/10.1007/978-3-319-98852-8_3

    Chapter  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Collins C (2015) A tutorial for discriminant analysis of principal components (DAPC) using Adegenet 2.0. 0. Imperial College London, MRC Centre for Outbreak Analysis and Modelling, London

    Google Scholar 

  • Kahilainen KK, Siwertsson A, Gjelland KØ, Knudsen R, Bøhn T, Amundsen P-A (2011) The role of gill raker number variability in adaptive radiation of coregonid fish. Evol Ecol 25:573–588

    Article  Google Scholar 

  • Komarova AS, Golubtsov AS, Levin BA (2022) Trophic diversification out of ancestral specialization: an example from a radiating African cyprinid fish (genus Garra). Diversity 14(8):629

    Article  CAS  Google Scholar 

  • Kottelat M (2020) Ceratogarra, a genus name for Garra cambodgiensis and G. fasciacauda and comments on the oral and gular soft anatomy in labeonine fishes (Teleostei: Cyprinidae). Raffles Bull Zool 35:156–178

    Google Scholar 

  • Lahti DC et al (2009) Relaxed selection in the wild. Tr Ecol Evol 24(9):487–496

    Article  Google Scholar 

  • Levin B, Simonov E, Franchini P, Mugue N, Golubtsov A, Meyer A (2021) Rapid adaptive radiation in a hillstream cyprinid fish in the East African White Nile River basin. Mol Ecol 30(21):5530–5550

    Article  CAS  PubMed  Google Scholar 

  • Mascher M, Wu S, Amand PS, Stein N, Poland J (2013) Application of genotyping-by-sequencing on semiconductor sequencing platforms: a comparison of genetic and reference-based marker ordering in barley. PLoS One 8(10):e76925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menon AGK (1964) Monograph of the cyprinid fishes of the genus Garra Hamilton, vol 14. https://faunaofindia.nic.in/PDFVolumes/memoirs/014/04/0173-0260.pdf

  • Mousavi-Sabet H, Eagderi S (2016) Garra lorestanensis, a new cave fish from the Tigris River drainage with remarks on the subterranean fishes in Iran (Teleostei: Cyprinidae). FishTaxa 1(1):45–54

    Google Scholar 

  • Muchlisin ZA (2014) A general overview on some aspects of fish reproduction. Aceh Internat J Sci Technol 3(1):43–52

    Article  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106(949):283–292

    Article  Google Scholar 

  • Patimar R, Chalanchi MG, Chamanara V, Naderi L (2010) Some life history aspects of Garra rufa (Heckel, 1843) in the Kangir River, Western Iran: (Osteichthyes: Cyprinidae). Zool Mid East 51(1):57–66

    Article  Google Scholar 

  • Pazira A-R, Moghdani S, Ghanbari F (2013) Age structure and growth of the Garra rufa (Cyprinidae), in southern Iran. Int J Biosci 3(12):115–119

    Article  Google Scholar 

  • Pembleton LW, Cogan NO, Forster JW (2013) St AMPP: An R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour 13(5):946–952

    Article  CAS  PubMed  Google Scholar 

  • Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209(12):2362–2367

    Article  PubMed  Google Scholar 

  • Poulson TL (1963) Cave adaptation in amblyopsid fishes. Am Midl Nat 70:257–290

    Article  Google Scholar 

  • Robinson BW, Wilson DS (1994) Character release and displacement in fishes: a neglected literature. Am Nat 144(4):596–627

    Article  Google Scholar 

  • Ronco F, Salzburger W (2021) Tracing evolutionary decoupling of oral and pharyngeal jaws in cichlid fishes. Evol Lett 5(6):625–635

    Article  PubMed  PubMed Central  Google Scholar 

  • Stiassny ML, Getahun A (2007) An overview of labeonin relationships and the phylogenetic placement of the Afro-Asian genus Garra Hamilton, 1922 (Teleostei: Cyprinidae), with the description of five new species of Garra from Ethiopia, and a key to all African species. Zool J Linnean Soc 150(1):41–83

    Article  Google Scholar 

  • Taylor EB (1999) Species pairs of north temperate freshwater fishes: evolution, taxonomy, and conservation. Rev Fish Biol Fish 9:299–324

    Article  Google Scholar 

Download references

Acknowledgements

This work is dedicated to Mr. Tayeb Hashemzadeh Segherloo and Mesdames Madeleine Drouin and Böyük-Khanim Ahmadi Segherloo. The authors thank Farokh Shirali of the Behbahan Bureau of Environment and Mohammad Taromi of the Qazvin Kavoshgaran Caving Club, who assisted the authors with sampling. We also thank the editor and two anonymous reviewers for their constructive comments on a previous version of our manuscript. This work was supported by a NSERC (Canada) Discovery grant (http://www.nserc-crsng.gc.ca) to Louis Bernatchez, grant number 688MIGRD94 to Iraj Hashemzadeh Segherloo by ShahreKord University (www.sku.ac.ir), and the University of Basrah. Sampling procedures comply with the current laws of Islamic Republic of Iran.

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Correspondence to Iraj Hashemzadeh Segherloo or Amaal Gh. Yasser.

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The ethical aspects and procedures applied in this research were approved under ethical code no IR.SKU.REC.1401.048 by the research ethics committee of ShahreKord University.

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Hashemzadeh Segherloo, I., Najafi Chaloshtory, S., Yasser, A.G. et al. Flexibility of life to survive limitations: oral disc forms in the Tashan Cave barb Garra tashanensis. Environ Biol Fish 106, 2083–2092 (2023). https://doi.org/10.1007/s10641-023-01475-1

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