Integrated Taxonomy Revealed Genetic Differences in Morphologically Similar and Non-Sympatric Scoliodon macrorhynchos and S. laticaudus

Simple Summary In this study, the species identities of similar-looking coastal spadenose sharks from different areas were clarified by adding new molecular markers and more individual body measurements, including animals from the Malaysian Peninsula that had not been examined previously. Collective evidence showed that there are two genetically distinct species that do not overlap in their spatial occurrence. The Malacca Strait acts as a boundary delineating the distribution range of the Pacific spadenose shark Scoliodon macrorhynchos to the east and, of the Northern Indian Ocean, S. laticaudus to the west. In addition, the need to determine the species status of Scoliodon animals from Indonesian waters was identified. The present study reinforced the need to rely on comprehensive genetic information in addition to external characteristics to assess the species identities and distribution range for small sharks and rays that have apparent contiguous coastal distribution with limited dispersal abilities. Abstract Previous examination of the mitochondrial NADH2 gene and morphological characteristics led to the resurrection of Scoliodon macrorhynchos as a second valid species in the genus, in addition to S. laticaudus. This study applied an integrated taxonomic approach to revisit the classification of the genus Scoliodon based on new materials from the Malaysian Peninsula, Malaysian Borneo and Eastern Bay of Bengal. Mitochondrial DNA data suggested the possibility of three species of Scoliodon in the Indo-West Pacific, while the nuclear DNA data showed partially concordant results with a monophyletic clade of S. macrorhynchos and paraphyletic clades of S. laticaudus and S. cf. laticaudus from the Malacca Strait. Morphological, meristic and dental characteristics overlapped between the three putative species. Collective molecular and morphological evidence suggested that the differences that exist among the non-sympatric species of Scoliodon are consistent with isolation by distance, and Scoliodon macrorhynchos remains as a valid species, while S. cf. laticaudus is assigned as S. laticaudus. The Malacca Strait acts as a spatial delineator in separating the Pacific S. macrorhynchos (including South China Sea) from the Northern Indian Ocean S. laticaudus. Future taxonomic work should focus on clarifying the taxonomic status of Scoliodon from the Indonesian waters.

[1]  Fahmi,et al.  Population structure of the brown-banded bamboo shark, Chiloscyllium punctatum and its relation to fisheries management in the Indo-Malay region , 2021 .

[2]  K. Loh,et al.  Brown banded bamboo shark (Chiloscyllium punctatum) shows high genetic diversity and differentiation in Malaysian waters , 2021, Scientific Reports.

[3]  M. Shiao,et al.  A review on the genetic structure of ecologically and economically important mangrove species in the Indo-West Pacific , 2021 .

[4]  G. Naylor,et al.  Integrative taxonomy identifies a new stingray species of the genus Hypanus Rafinesque, 1818 (Dasyatidae, Myliobatiformes) from the Tropical Southwestern Atlantic. , 2020, Journal of fish biology.

[5]  Andrés Martin,et al.  Yearbook , 2019, Journal of the American Academy of Child & Adolescent Psychiatry.

[6]  U. Waqas,et al.  A first account of the elasmobranch fishery of Balochistan, south-west Pakistan , 2019, Western Indian Ocean Journal of Marine Science.

[7]  U. Zajonz,et al.  Coastal fish diversity of the Socotra Archipelago, Yemen. , 2019, Zootaxa.

[8]  Bin Ye,et al.  Enigmatic incongruence between mtDNA and nDNA revealed by multi-locus phylogenomic analyses in freshwater snails , 2019, Scientific Reports.

[9]  D. Ebert,et al.  New insights into the identities of the elasmobranch fauna of Sri Lanka. , 2019, Zootaxa.

[10]  T. Arai,et al.  Diversity, occurrence and conservation of sharks in the southern South China Sea , 2019, PloS one.

[11]  Maryam Rabiee,et al.  Multi-allele species reconstruction using ASTRAL , 2018, bioRxiv.

[12]  K. Chu,et al.  Contrasting population genetic structure in three aggregating groupers (Percoidei: Epinephelidae) in the Indo-West Pacific: the importance of reproductive mode , 2018, BMC Evolutionary Biology.

[13]  K. Bineesh,et al.  First report of four deep-sea chondrichthyans (Elasmobranchii and Holocephali) from Andaman waters, India with an updated checklist from the region , 2018, Acta Ichthyologica et Piscatoria.

[14]  R. Jabado,et al.  New records of sharks (Elasmobranchii) from the Andaman and Nicobar Archipelago in India with notes on current checklists , 2018, Biodiversity data journal.

[15]  Xiyun Jiao,et al.  Species Tree Inference with BPP Using Genomic Sequences and the Multispecies Coalescent , 2018, Molecular biology and evolution.

[16]  Chao Zhang,et al.  ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees , 2018, BMC Bioinformatics.

[17]  W. White,et al.  Catch composition and aspects of the biology of sharks caught by Thai commercial fisheries in the Andaman Sea. , 2018, Journal of fish biology.

[18]  G. Naylor,et al.  Redescription of Chimaera ogilbyi (Chimaeriformes; Chimaeridae) from the Indo-Australian region. , 2018, Zootaxa.

[19]  R. Ward,et al.  DNA barcoding reveals species composition of sharks and rays in the Indian commercial fishery , 2017, Mitochondrial DNA. Part A, DNA mapping, sequencing, and analysis.

[20]  A. Widodo,et al.  SUMBERDAYA IKAN CUCUT (HIIJ) YANG TERTANGKAP NELAYAN DI PERAIRAN L AUT JAWA [The shark resource caught by fishermen in Java Sea] , 2017 .

[21]  E. M. Abdussamad,et al.  Check list of fishes of the Gulf ofMannar ecosystem, Tamil Nadu, India , 2016 .

[22]  Dharmadi,et al.  Genetic and phenotypic diversity in the wedgefish Rhynchobatus australiae, a threatened ray of high value in the shark fin trade , 2016 .

[23]  B. Rannala,et al.  Efficient Bayesian Species Tree Inference under the Multispecies Coalescent , 2015, Systematic biology.

[24]  R. Jabado,et al.  Shark diversity in the Arabian/Persian Gulf higher than previously thought: insights based on species composition of shark landings in the United Arab Emirates , 2015, Marine Biodiversity.

[25]  Ziheng Yang,et al.  Unguided Species Delimitation Using DNA Sequence Data from Multiple Loci , 2014, Molecular biology and evolution.

[26]  Roy,et al.  Landing Trends, Species composition and Percentage composition of Sharks and Rays in Chittagong and Cox's Bazar, Bangladesh , 2014 .

[27]  G. Naylor,et al.  An annotated checklist of the chondrichthyans of Taiwan. , 2013, Zootaxa.

[28]  R. Peirce,et al.  Composition of elasmobranch landings in Bahrain , 2013 .

[29]  L. Compagno,et al.  Sharks of the World: A Fully Illustrated Guide , 2013 .

[30]  Mahendra D. Fofandi,et al.  Observations on selected biological aspects of the spadenose shark (Scoliodon laticaudus Müller & Henle, 1838), landed along Saurashtra coast , 2013 .

[31]  N. Andreakis,et al.  Phylogeography of the Indo-West Pacific maskrays (Dasyatidae, Neotrygon): a complex example of chondrichthyan radiation in the Cenozoic , 2012, Ecology and evolution.

[32]  D. Silvestro,et al.  raxmlGUI: a graphical front-end for RAxML , 2012, Organisms Diversity & Evolution.

[33]  G. Naylor,et al.  A DNA Sequence–Based Approach To the Identification of Shark and Ray Species and Its Implications for Global Elasmobranch Diversity and Parasitology , 2012 .

[34]  Neil C. Aschliman,et al.  Phylogeny of Batoidea , 2012 .

[35]  G. Carvalho,et al.  Species, sex, size and male maturity composition of previously unreported elasmobranch landings in Kuwait, Qatar and Abu Dhabi Emirate. , 2012, Journal of fish biology.

[36]  Vivian Y Y Lam,et al.  The sharks of South East Asia – unknown, unmonitored and unmanaged , 2011 .

[37]  Dharmadi,et al.  Sharks and Rays of Borneo , 2010 .

[38]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[39]  F. Balloux The worm in the fruit of the mitochondrial DNA tree , 2010, Heredity.

[40]  Caitlin A. Kuczynski,et al.  Discordant mitochondrial and nuclear gene phylogenies in emydid turtles: implications for speciation and conservation , 2010 .

[41]  N. Galtier,et al.  Mitochondrial DNA as a marker of molecular diversity: a reappraisal , 2009, Molecular ecology.

[42]  A. Henderson,et al.  Size distributions and sex ratios of sharks caught by Oman's artisanal fishery , 2009 .

[43]  Todd A. Castoe,et al.  Evidence for an ancient adaptive episode of convergent molecular evolution , 2009, Proceedings of the National Academy of Sciences.

[44]  R. Ward,et al.  DNA barcoding Australasian chondrichthyans: results and potential uses in conservation , 2008 .

[45]  N. Galtier,et al.  Strong variations of mitochondrial mutation rate across mammals--the longevity hypothesis. , 2007, Molecular biology and evolution.

[46]  W. White Catch composition and reproductive biology of whaler sharks (Carcharhiniformes: Carcharhinidae) caught by fisheries in Indonesia , 2007 .

[47]  Akifumi S. Tanabe,et al.  kakusan: a computer program to automate the selection of a nucleotide substitution model and the configuration of a mixed model on multilocus data , 2007 .

[48]  J. McIlwain,et al.  The Sultanate of Oman shark fishery: Species composition, seasonality and diversity , 2007 .

[49]  P. Higgs,et al.  The Relationship Between the Rate of Molecular Evolution and the Rate of Genome Rearrangement in Animal Mitochondrial Genomes , 2006, Journal of Molecular Evolution.

[50]  D. Littlewood,et al.  Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo‐West Pacific , 2006 .

[51]  Nicolas Galtier,et al.  Population Size Does Not Influence Mitochondrial Genetic Diversity in Animals , 2006, Science.

[52]  Michael K. Musyl,et al.  Shipboard identification of fish eggs and larvae by multiplex PCR, and description of fertilized eggs of blue marlin, shortbill spearfish, and wahoo , 2005 .

[53]  K. Strimmer,et al.  TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics , 2004, BMC Evolutionary Biology.

[54]  J. Bishop History and current checklist of Kuwait's ichthyofauna , 2003 .

[55]  R. Hall Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations , 2002 .

[56]  D. Rand THE UNITS OF SELECTION ON MITOCHONDRIAL DNA , 2001 .

[57]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[58]  P. Awadalla,et al.  Linkage disequilibrium and recombination in hominid mitochondrial DNA. , 1999, Science.

[59]  E. Hagelberg,et al.  Evidence for mitochondrial DNA recombination in a human population of island Melanesia , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  A. Eyre-Walker,et al.  How clonal are human mitochondria? , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[61]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[62]  C. Rao Scientific, common and local names of commercially important edible marine fin and shell fishes of Andhra Pradesh , 1991 .

[63]  L. Compagno,et al.  Sharks of the Order Carcharhiniformes , 1988 .

[64]  Mukhtar Ahmad,et al.  Studies on Sharks-XIV. Reproduction in the Telok Anson Shark Collected from Perak River, Malaysia , 1978 .

[65]  V. G. Springer A revision of the carcharhinid shark genera Scoliodon, Loxodon, and Rhizoprionodon , 1964 .

[66]  K. S. Misra An Aid to the Identification of the Common Commercial Fishes of India and Pakistan , 1959, Records of the Zoological Survey of India.

[67]  K. S. Misra A Check list of the Fishes of India, Burma and Ceylon. Part I. Elasmobranchii and Holocephali , 1947, Records of the Zoological Survey of India.

[68]  Barton A. Bean,et al.  Notes on a collection of fishes from Java, made by Owen Bryant and William Palmer in 1909, with description of a new species , 1912 .

[69]  G. Dash,et al.  Overview of elasmobranch fisheries of WestBengal in 2018 , 2018 .

[70]  D. Swofford,et al.  Phylogeny of the manta and devilrays (Chondrichthyes: mobulidae), with an updated taxonomic arrangement for the family , 2018 .

[71]  A. Moore,et al.  Sharks and rays of the Arabian/Persian Gulf , 2015 .

[72]  Kenyan Coast,et al.  SHARK BYCATCH - SMALL SCALE TUNA FISHERY INTERACTIONS ALONG THE , 2013 .

[73]  T. Sujitha,et al.  Case of leucism in the spadenose shark, Scoliodon laticaudus (Müller and Henle, 1838) from Mangalore, Karnataka , 2011 .

[74]  Li Yan Preliminary study on biological characteristics of spadenose shark,Scoliodon laticaudus,caught from coastal waters of Zhejiang province , 2008 .

[75]  G. Naylor,et al.  Phylogenetic Relationships among the Major Lineages of Modern Elasmobranchs , 2004 .

[76]  中坊 徹次,et al.  Fishes of Japan : with pictorial keys to the species , 2002 .

[77]  K. Carpenter FAO Species Identification Guide for Fishery Purposes , 2002 .

[78]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[79]  P. Pillai,et al.  Pelagic Sharks in the Indian Seas their Exploitation, Trade, Management and Conservation , 2000 .

[80]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[81]  M. Esseen,et al.  Occurrence and distribution of fish species off Yemen (Gulf of Aden and Arabian Sea) , 1999 .

[82]  J. Morón,et al.  A check-list of sharks and rays of western Sri Lanka , 1998 .

[83]  K. Udupa,et al.  LENGTH-WEIGHT RELATIONSHIP OF SCOLIODONLATICAUDUS MULLER AND HENLE AND CARCHARHINUS LIMBATUS (MULLER AND HENLE), FROM DAKSHINA KANNADA COAST , 1988 .

[84]  L. Compagno,et al.  Sharks of the world :an annotated and illustrated catalogue of shark species known to date , 1984 .

[85]  R. Nair,et al.  On the Systematics and identity of four pelagicSharks of the family Carcharhinidaefrom Indian region , 1974 .

[86]  P. Talwar CONTRIBUTION TO THE TAXONOMY OF RHIZOPRIONODON OLIGOLINX SPRINGER 1964: AN IMPORTANT COMPONENT OF THE SHARK FISHERY OF ORISSA, INDIA , 1974 .

[87]  V. G. Springer,et al.  A Survey of Vertebral Numbers in Sharks , 1964 .

[88]  J. Müller,et al.  Systematische Beschreibung der Plagiostomen , 1841 .