Abstract
Globally, many of the Elasmobranch species are threatened with extinction due to their vulnerable life history traits, habitat alterations, overexploitation, and climate change. The Spadenose shark, Scoliodon laticaudus Müller & Henle, 1838, is an amphidromous coastal shark that exhibits placental viviparity. The latest IUCN Red List of Threatened species classified S. laticaudus as near threatened (NT) indicating its vulnerability to overfishing. We investigated the genetic population structure of S. laticaudus along the Indian coast using mitochondrial cytochrome C Oxidase 1 (COI), control region, and NADH dehydrogenase subunit 2 (NADH2) markers. Significant genetic differentiation was detected between the east and west coasts of India with the occurrence of two major haplotypes, one dominant along the east coast, and the other along the west coast when analyzed using all the 3 markers. The NADH2 sequences of the predominant haplotype from the west coast recorded 100% identity with sequences of S. laticaudus deposited in NCBI, GenBank. On the contrary, the predominant haplotype from the east coast recorded 100% identity with sequences of Scoliodon cf. laticaudus deposited in NCBI, GenBank. The divergence values of 2% and 3.7% between these haplotypes in the COI and NADH2 genes, respectively, indicate that they can be considered distinct species. Divergence between populations and speciation indicates restricted mixing and gene flow due to the limited dispersal capacity of nearshore elasmobranchs. Natal philopatry, selection on mitochondrial genes due to differential habitat characteristics, and environmental differences between the east and west coasts of India can also be considered as reasons for restricted gene flow and genetic differentiation. Based on the results of the present study, S. laticaudus and the putative S. cf. laticaudus can be managed separately along the Indian coast. A comprehensive investigation based on morphological and molecular information is also warranted to resurrect S. cf. laticaudus as a new species. Besides, restrictions on the fishery and the use of bycatch reduction devices in trawls can be undertaken to conserve this species from further depletion and possible extinction in the future.
This is a preview of subscription content, log in via an institution to check access.
References
Biais G, Coupeau Y, Séret B, Calmettes B, Lopez R, Hetherington S, Righton D (2017) Return migration patterns of porbeagle shark (Lamna nasus) in the Northeast Atlantic: implications for stock range and structure. ICES J Mar Sci 74:1268–1276. https://doi.org/10.1093/icesjms/fsw233
Bleeker PR (1852) Bijdrage tot de kennis der Plagiostomen van den Indischen Archipel. Verh Batav Genoot Kunst Wet 24(12):1–92
Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annu Rev Mar Sci 7(1):547–570. https://doi.org/10.1146/annurev-marine-010814-015730
Chatterjee A, Shankar D, Sheno SSC, Reddy GV, Michael GS, Ravichandran M, Gopalkrishna VV, Ramrao EP, Udayabhaskar TVS, Sanjeevan VN (2012) A new atlas of temperature and salinity for the North Indian Ocean. J Earth Syst Sci 121:559–593. https://doi.org/10.1007/s12040-012-0191-9
Compagno LJV (1984) FAO Species Catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2 - Carcharhiniformes. FAO Fish Synop 125(4/2):251-655. FAO, Rome (Ref. 244)
Compagno LJV (2005) Global checklist of living chondrichthyan fishes. In: Fowler SL, Cavanagh RD (eds) Sharks, rays and chimaeras: the status of chondrichthyan fishes. International Union for the Conservation of Nature and Natural Resources, Cambridge, pp 401–423
Daly-Engel TS, Seraphin KD, Holland KN, Coffey JP, Nance HA, Toonen RJ, Bowen BW (2012) Global Phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini). PLoS ONE 7(1):e29986. https://doi.org/10.1371/journal.pone.0029986
Devadoss P (1979) Observations on the maturity, breeding and development of Scoliodon laticaudus Müller and Henle off Calicut coast. J Mar Biol Ass India 21:103–110
Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LNK, Fordham SV, Francis MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE, Compagno LJV, Ebert DA, Gibson C, Heupel MR, Livingstone SR et al (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3:e00590. https://doi.org/10.7554/eLife.00590
Dulvy NK, Simpfendorfer C, Akhilesh KV, Derrick D, Elhassan I, Fernando D, Haque AB, Jabado RW, Maung A, Valinassab T et al (2021) Scoliodon laticaudus. The IUCN Red List of Threatened Species. Available online: https://doi.org/10.2305/IUCN.UK.2021-2.RLTS.T169234201A173436322.en. Accessed 14 Dec 2021
Ebert DA, Dando M, Fowler S (2021) Sharks of the world: a complete guide. Princeton University Press, Princeton
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 13:479–491. https://doi.org/10.1093/genetics/131.2.479
Excoffier L, Laval G, Schneider S (2007) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299
Hauser L, Turan C, Carvalho GR (2001) Haplotype frequency distribution and discriminatory power of two mtDNA fragments in a marine pelagic teleost (Atlantic herring, Clupea harengus). Heredity 87:621–630. https://doi.org/10.1046/j.1365-2540.2001.00956.x
IUCN (2017) The IUCN red list of threatened species. Version 2017-1. www.iucnredlist.org. Downloaded on 18 May 2017
Leigh JW, Bryant D (2015) popart: full-feature software for haplotype network construction. Methods Ecol Evol. https://doi.org/10.1111/2041-210X.12410
Lim KC, White WT, Then AYH, Naylor GJP, Arunrugstichai S, Loh KH (2022) Integrated taxonomy revealed genetic differences in morphologically similar and non-sympatric Scoliodon macrorhynchos and S. laticaudus. Animals (Basel) 12(6):681. https://doi.org/10.3390/ani12060681
Mohamed KS, Veena S (2016) How long does it take for tropical marine fish stocks to recover after declines? Case studies from the Southwest coast of India. Curr Sci 110(4):584–594
Morgan JAT, Harry AV, Welch DJ, Street R, White J, Geraghty PT, Macbeth WG, Tobin A, Simpfendorfer CA, Ovenden JR (2011) Detection of interspecies hybridisation in Chondrichthyes: hybrids and hybrid offspring between Australian (Carcharhinus tilstoni) and common (C. limbatus) blacktip shark found in an Australian fishery. Conserv Genet 13:455–463. https://doi.org/10.1007/s10592-011-0298-6
Müller J, Henle FGJ (1837) Ueber die Gattungen der Plagiostomen. Archiv für Naturgeschichte 3:394–401
Müller J, Henle FGJ (1838) On the generic characters of cartilaginous fishes, with descriptions of new genera. Magazine of Natural History and Journal of Zoology, Botany, Mineralogy, Geology, and Meteorology, (n.s.) 2:33–37; 88–91
Naylor G, Caira JN, Jensen K, Rosana KAM, White W, Last P (2012) A DNA sequence based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bull Am Mus Nat Hist 367:1–262. https://doi.org/10.1206/754.1
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. https://doi.org/10.1111/j.1558-5646.1989.tb04220.x
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analysis by the coalescent and other methods. Bioinformatics 19:2496–2497. https://doi.org/10.1093/bioinformatics/btg359
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, New York
Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory. University of Geneva, Geneva
Sen S, Chakraborty SK, Zacharia PU, Dash G, Kizhakudan SJ, Bharadiya SA, Gohel JK (2018) Reproductive strategy of spadenose shark, Scoliodon laticaudus Müller and Henle, 1839 along north-eastern Arabian Sea. J Appl Ichthyol 34:1304–1313. https://doi.org/10.1111/jai.13794
Straube N, White WT, Ho HC, Rochel E, Corrigan S, Li C, Naylor GJ (2013) A DNA sequence-based identification checklist for Taiwanese chondrichthyans. Zootaxa 3752:256–278. https://doi.org/10.11646/zootaxa.3752.1.16
Thomas S, Purushottama GB, Nataraja GD, Kizhakudan SJ (2020) Fishery and biological characteristics of the spadenose shark Scoliodon laticaudus Müller & Henle, 1838 from the Eastern Arabian Sea. Reg Stud Mar Sci 34. https://doi.org/10.1016/j.rsma.2020.101085
Weigmann (2016) Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. J Fish Biol 88(3):837–1037. https://doi.org/10.1111/jfb.12874
White WT, Last PR, Naylor GJP (2010) Scoliodon macrorhynchos (Bleeker, 1852), a second species of spadenose shark from the western Pacific (Carcharhiniformes: Carcharhinidae). In: Last PR, White WT, Pogonoski JJ (eds) Descriptions of new sharks and rays from Borneo: 61–76. CSIRO Marine and Atmospheric Research Paper 032, Hobart
Acknowledgements
The authors would like to thank Dr. P. Vijayagopal (Head, Marine Biotechnology Division, CMFRI), and Director, CMFRI for providing facilities for carrying out this work. This work was carried out under the institute projects DEM/ELS/11 and MBT/GNM/25 receiving funding support from the Indian Council of Agricultural Research (ICAR). The EAF-Nansen Programme implemented by the Food and Agriculture Organization of the United Nations (FAO) in close collaboration with the Norwegian Institute of Marine Research (IMR) and funded by the Norwegian Agency for Development Cooperation (Norad), provided the opportunity for AKV to participate in the 2018 Myanmar survey aboard the R/V Dr. Fridtjof Nansen and examine photographs/specimens/ and collect samples of Scoliodon. We acknowledge the support of Kathrine Michalsen (IMR), Htun Thein (Department of Fisheries, Myanmar), and the crew and personnel involved in the above-mentioned survey. We would also like to thank the anonymous reviewers for their constructive suggestions to improve the quality of the manuscript.
Funding
The study received funding support from the Indian Council of Agricultural Research (ICAR).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals have been followed by the authors.
Sampling and field studies
All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable. The study is compliant with CBD and Nagoya protocols.
Data availability
All data generated during this study are included in this published article. Information regarding sequences generated out of the present study has been deposited in NCBI, GenBank.
Author contributions
SS: conceptualization, design, funding acquisition, research work, methodology, analysis, writing. WS: lab work, methodology, analysis, writing. PUZ: funding acquisition, review. SJK: conceptualization, funding acquisition, sample collection, writing. AKV: conceptualization, sample collection, writing. ST: conceptualization, sample collection, writing. SKR, MM, SPS, PGB, SR, BKK, KTG: sample collection, writing. AG: funding acquisition, review.
Additional information
Communicated by S. Weigmann
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 25.5 kb)
Rights and permissions
About this article
Cite this article
Sukumaran, S., Sebastian, W., Zacharia, P.U. et al. Population genetic research on the Spadenose shark, Scoliodon laticaudus (Chondrichthyes, Carcharhinidae), reveals the presence of two significantly differentiated clades along the Indian coast. Mar. Biodivers. 53, 16 (2023). https://doi.org/10.1007/s12526-022-01324-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12526-022-01324-x