Abstract
Among Tashan cave barb Garra tashanensis inhabiting a small cave in southwest Iran, two mental disc (sucking mouth disc) forms were observed. To assess their phylogenetic relationships, disc-less and disc-bearing individuals were analyzed using mitochondrial cytochrome oxidase subunit I (COI) partial DNA sequences. Both mental disc forms nested within one clade with absolute bootstrap support (BS = 100), and the genetic distances between the disc-bearing and disc-less individuals (0.3–0.8%) were considerably lower than inter-species mtDNA sequence distances reported among members of the genus Garra; further, most species delimitation algorithms used here showed disc-bearing and disc-less Tashan cave barbs to be members of a single taxonomic unit. Hence, the observed mental disc variation was not inferred to be a taxonomic feature or a consequence of character displacement. Instead, it was inferred to be a case of character release to diversify among ecological niches in the limited subterranean habitat or a case of relaxed selection, which should be clarified in detail in follow-up ecological and population genetic studies.
Data availability
All sequences and their complementary data related to this study are available under GenBank accession numbers: ON203035-ON203041 and under BOLD TASH project.
References
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
Ashraf S, Nazemi A, AghaKouchak A (2021) Anthropogenic drought dominates groundwater depletion in Iran. Sci Rep 11(1):9135. https://doi.org/10.1038/s41598-021-88522-y
Bagheri M, Goudarzi F, Zalaghi AH, Savabieasfahani M (2016) Habitat characteristics and population size of Iranocypris typhlops, the Iran cave barb. Environ Biol Fishes 99(2):179–185
Clement M, Snell Q, Walker P, Posada D, Crandall K (2002) TCS: estimating gene genealogies. Parallel Distributed Process Symp Int Proc 3:184
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772
Davis J, Pavlova A, Thompson R, Sunnucks P (2013) Evolutionary refugia and ecological refuges: key concepts for conserving Australian arid zone freshwater biodiversity under climate change. Global Change Biol 19(7):1970–1984
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797
Endo C, Watanabe K (2020) Morphological variation associated with trophic niche expansion within a lake population of a benthic fish. PloS one 15(4): p.e0232114
Esmaeili HR, Sayyadzadeh G, Eagderi S (2016) Review of the genus Garra Hamilton, 1822 in Iran with description of a new species: a morpho-molecular approach (Teleostei: Cyprinidae). Iran J Ichthyol 3(2):82–121
Fagan B (2014) The attacking ocean: the past, present, and future of rising sea levels. Bloomsbury Publishing, New York, p 288
Farashi A, Kaboli M, Rezaei HR, Naghavi MR, Rahimian H, Coad BW (2014) Reassessment of the taxonomic position of Iranocypris typhlops Bruun and Kaiser, 1944 (Actinopterygii, Cyprinidae). ZooKeys 374:69–77
Freyhof J, Abdullah YS, Ararat K, Ibrahim H, Geiger MF (2016) Eidinemacheilus proudlovei, a new subterranean loach from Iraqi Kurdistan (Teleostei; Nemacheilidae). Zootaxa 4173(3):225–236
Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol 62:707–724
Gray S, Robinson B, Parsons K (2005) Testing alternative explanations of character shifts against ecological character displacement in brook sticklebacks (Culaea inconstans) that coexist with ninespine sticklebacks (Pungitius pungitius). Oecologia 146(1):25–35
Hall TA (2014) BioEdit version 7.2.5. http://bioedit.software.informer.com/.
Hallerman EM (2003) Population genetics: principles and applications for fisheries scientists. American Fisheries Society, Bethesda (Maryland), p 458
Hashemzadeh Segherloo I, Bernatchez L, Golzarianpour K, Abdoli A, Primmer CR, Bakhtiary M (2012) Genetic differentiation between two sympatric morphs of the blind Iran cave barb Iranocypris typhlops. J Fish Biol 81(5):1747–1753
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. Modern Genetics 8(1):59–66
Hashemzadeh Segherloo I, Ghaedrahmati N, Freyhof J (2016) Eidinemacheilus, a new generic name for Noemacheilus smithi Greenwood (Teleostei; Nemacheilidae). Zootaxa 4147(4):466–476
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 gular sucking disc in Garra (Teleostei: Cyprinidae) in the Middle East. Hydrobiologia 785(1):47–59
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
Hashemzadeh Segherloo I, Tabatabaei SN, Abdolahi-Mousavi E, Hernandez C, Normandeau E, Laporte M, Boyle B, Amiri M, GhaedRahmati N, Hallerman E, Bernatchez L (2021) eDNA metabarcoding as a means to assess distribution of subterranean fish communities: Iranian blind cave fishes as a case study. Environ DNA 4(2):402–4016
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res. 36(Suppl_2):W5–W9
Kapli T, Lutteropp S, Zhang J, Kobert K, Pavlidis P, Stamatakis A, Flouri T (2016) Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33(11):1630–1638. https://doi.org/10.1093/bioinformatics/btx025
Kiani F, Hashemzadeh Segherloo I, Abdoli A, Shaloee F, Nikukhah F (2017) Phylogenetic analysis of the genus Garra in Karun, Karkheh, Dez, Tigris, and Mond Basins (Iran) using cytochrome oxidase subunit I. Modern Genetics 12(1):61–69
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874
Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, Coss RG, Donohue K, Foster SA (2009) Relaxed selection in the wild. Trends Ecol Evol 24(9):487–496
Lara A, Ponce de León JL, Rodriguez R, Casane D, Cote G, Bernatchez L, García-Machado E (2010) DNA barcoding of Cuban freshwater fishes: evidence for cryptic species and taxonomic conflicts. Mol Ecol Resour 10(3):421–430
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
Menon AGK (1964) Monograph of the cyprinid fishes of the genus Garra Hamilton. Memoirs Indian Museum 14(4):173–260
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
Mousavi-Sabet H, Vatandoust S, Fatemi Y, Eagderi S (2016) Tashan Cave, a new cave fish locality for Iran; and Garra tashanensis, a new blind species from the Tigris River drainage (Teleostei: Cyprinidae). FishTaxa 1(3):133–148
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290
Pfennig DW, Pfennig KS (2010) Character displacement and the origins of diversity. Am Nat 176(Suppl 1):S26
Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609
Puillandre N, Brouillet S, Achaz G (2021) ASAP: assemble species by automatic partitioning. Mol Ecol Resour 21(2):609–620
Robinson BW, Wilson DS (1994) Character release and displacement in fishes: a neglected literature. Am Nat 144(4):596–627
Robinson BW, Pfennig DW (2013) Inducible competitors and adaptive diversification. Curr Zool 59(4):537–552
Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, GuiraoRico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34:3299–3302
Sargeran P, Bakhtiyari M, Abdoli A, Coad BW, Sarvi K, Lishi MR, Hajimoradloo A (2008) The endemic Iranian cave-fish, Iranocypris typhlops: two taxa or two forms based on the mental disc? Zool Middle East 44(1):67–74
Schluter D (2000) The Ecology of Adaptive Radiation. Oxford University Press, Oxford
Stiassny MLJ, 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 Linn Soc 150(1):41–83
Zamani-Faradonbe M, Keivany Y, Dorafshan S, Zhang E (2021) Two new species of Garra (Teleostei: Cyprinidae) from western Iran. Ichthyol Explor Freshw 30(1):249–270
Zhang E (2005) Phylogenetic relationships of labeonine cyprinids of the disc-bearing group (Pisces: Teleostei). Zool Studies 44(1):130–143
Zhou W, Pan X-F, Kottelat M (2005) Species of Garra and Discogobio (Teleostei: Cyprinidae) in the Yuanjiang (Upper Red River) drainage of Yunnan Province, China with a description of a new species. Zool Studies Taipei 44(4):445
Acknowledgements
This work is dedicated to Mesdames Madeleine Drouin and Böyük-Khanim Ahmadi Segherloo. The authors thank Farokh Shirali of the Bahbahan Bureau of Environment and Mohammad Taromi of the Qazvin Kavoshgaran Caving club, who assisted the authors for 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, a grant from the Mohamed bin Zayed (MBZ) Species Conservation Fund (Project 172514955; https://www.speciesconservation.org) and 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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Hashemzadeh Segherloo, I., Najafi Chaloshtory, S., Naser, M.D. et al. Sympatric morphotypes of the restricted-range Tashan Cave Garra: distinct species or a case of phenotypic plasticity?. Environ Biol Fish 105, 1251–1260 (2022). https://doi.org/10.1007/s10641-022-01329-2
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DOI: https://doi.org/10.1007/s10641-022-01329-2