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Multiple Cryptic Species in the Blue-Spotted Maskray (Myliobatoidei: Dasyatidae: Neotrygon Spp.)

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Multiple Cryptic Species in the Blue-Spotted Maskray (Myliobatoidei: Dasyatidae: Neotrygon Spp.) View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector C. R. Biologies 339 (2016) 417–426 Contents lists available at ScienceDirect Comptes Rendus Biologies ww w.sciencedirect.com Taxonomy/Taxinomie Multiple cryptic species in the blue-spotted maskray (Myliobatoidei: Dasyatidae: Neotrygon spp.): An update Espe`ces cryptiques multiples chez la pastenague masque´e a` points bleus (Myliobatoidei : Dasyatidae : Neotrygon spp.) : actualisation a, b c d Philippe Borsa *, Kang-Ning Shen , Irma S. Arlyza , Thierry B. Hoareau a Institut de recherche pour le de´veloppement (IRD), Oceans department, Marseille, France b Department of Environmental Biology and Fisheries Science, National Taiwan Ocean University, Keelung, Taiwan c Lembaga Ilmu Pengetahuan Indonesia (LIPI), Pusat Penelitian Oseanografi (P2O), Jakarta, Indonesia d Molecular Ecology and Evolution Programme, Department of Genetics, University of Pretoria, Pretoria, South Africa A R T I C L E I N F O A B S T R A C T Article history: Previous investigations have uncovered divergent mitochondrial clades within the blue- Received 4 April 2016 spotted maskray, previously Neotrygon kuhlii (Mu¨ ller and Henle). The hypothesis that the Accepted after revision 19 July 2016 blue-spotted maskray may consist of a complex of multiple cryptic species has been Available online 16 August 2016 proposed, and four species have been recently described or resurrected. To test the multiple cryptic species hypothesis, we investigated the phylogenetic relationships and Keywords: coalescence patterns of mitochondrial sequences in a sample of 127 new individuals from Parapatric distribution the Indian Ocean and the Coral Triangle region, sequenced at both the CO1 and cytochrome Neotrygon kuhlii b loci. The maximum-likelihood (ML) tree of concatenated CO1 + cytochrome b gene Neotrygon trigonoides sequences, rooted by the New Caledonian maskray N. trigonoides, yielded 9 strongly Indo-West Pacific supported, main clades. Puillandre’s ABGD algorithm detected gaps in nucleotide distance Coral Triangle consistent with the ML phylogeny. The general mixed Yule-coalescent algorithm partitioned the dataset into putative species generally consistent with the ML phylogeny. Nuclear markers generally confirmed that distinct mitochondrial clades correspond to genetically isolated lineages. The nine main lineages identified by ML analysis were geographically distributed in a parapatric fashion, indicating reproductive isolation. The hypothesis of multiple cryptic species is thus validated. ß 2016 Acade´mie des sciences. Published by Elsevier Masson SAS. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/ 4.0/). R E´ S U M E´ Mots cle´s : Des recherches ante´rieures ont montre´ des clades mitochondriaux divergents chez la raie Distribution parapatrique masque´e a` points bleus, pre´ce´demment appele´e Neotrygon kuhlii (Mu¨ ller et Henle). Neotrygon kuhlii L’hypothe`se d’un complexe d’espe`ces cryptiques chez la raie masque´e a` points bleus a e´te´ Neotrygon trigonoides propose´e ; trois espe`ces ont e´te´ re´cemment de´crites et une quatrie`me, ressuscite´e. Afin de Indo-Pacifique ouest tester l’hypothe`se d’espe`ces cryptiques multiples, nous e´tudions les relations phyloge´- Triangle du corail ne´tiques et les patrons de coalescence des se´quences mitochondriales d’un e´chantillon de 127 individus de l’oce´an Indien et de la re´gion du Triangle du corail, se´quence´s * Corresponding author. Institut de recherche pour le de´veloppement (IRD), UMR 250 ‘‘E´ cologie marine tropicale des oce´ans Pacifique et Indien’’, c/o Indonesian Biodiversity Research Center, Universitas Udayana, Jl Raya Sesetan Gang Markisa, 80322 Denpasar, Indonesia. E-mail addresses: [email protected], [email protected] (P. Borsa). http://dx.doi.org/10.1016/j.crvi.2016.07.004 1631-0691/ß 2016 Acade´mie des sciences. Published by Elsevier Masson SAS. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). 418 P. Borsa et al. / C. R. Biologies 339 (2016) 417–426 simultane´ment aux locus CO1 et cytochrome b. L’arbre de maximum de vraisemblance (ML) des se´quences partielles concate´ne´es des ge`nes CO1 et cytochrome b, racine´ par la raie masque´e de Nouvelle-Cale´donie N. trigonoides, montre neuf clades principaux ` fortement soutenus. A l’aide de l’algorithme ABGD de Puillandre, des lacunes dans la distribution des distances nucle´otidiques sont de´tecte´es, qui s’ave`rent ge´ne´ralement cohe´rentes avec la phyloge´nie de ML. L’algorithme mixte de Yule-coalescent (GYMC) partitionne l’ensemble de donne´es en un certain nombre d’espe`ces putatives, dont la de´limitation est ge´ne´ralement cohe´rente avec la phyloge´nie de ML. Les marqueurs nucle´aires confirment, en ge´ne´ral, que les clades mitochondriaux distincts caracte´risent des ligne´es ge´ne´tiquement isole´es. Les neuf ligne´es principales identifie´es par l’analyse de ML montrent une distribution parapatrique, ce qui indique qu’elles sont reproductivement isole´es. L’hypothe`se d’espe`ces cryptiques multiples est donc valide´e. ß 2016 Acade´mie des sciences. Publie´ par Elsevier Masson SAS. Cet article est publie´ en Open Access sous licence CC BY-NC-ND (http://creativecommons.org/licenses/by-nc-nd/ 4.0/). 1. Introduction and on the population genetic structure and phylogeo- graphy of the blue-spotted maskray [18,19]. Additional Taxonomic studies of sharks and rays have led to an mitochondrial clades have been uncovered within the upsurge in new species descriptions within the last decade blue-spotted maskray [15,17,19]. These clades have a ([1,2]; and references therein). In particular, it appears that parapatric-like distribution [19]. Meanwhile, molecular the number of species in the Coral Triangle region has been markers have advanced the systematics of species in the considerably under-estimated until recently [1]. Mean- genus Neotrygon: cryptic species have been uncovered while, grave concern has been expressed over the risk of within N. ningalooensis and N. picta [17], and the New extinction in shallow-water species from a number of Caledonian maskray N. trigonoides (Castelnau, 1873) [20] shark and ray families including Dasyatidae or stingrays. has been resurrected [16,21]. The hypothesis that the Overfishing of stingrays is particularly severe in the Coral blue-spotted maskray may itself consist of a complex of Triangle region [3–5] and management is urgently needed. multiple species has been raised repeatedly [14,15,17,22] Species are the fundamental units in many studies of and was also discussed by us [19,23]. We emphasized that biogeography, community ecology and conservation ecol- the parapatric-like population structure uncovered in the ogy. Both conservation and fisheries management require Coral Triangle region ‘‘points to incipient speciation, where that species be clearly identified and populations be some degree of reproductive isolation has been achieved but delineated [6]. ecological compatibility has not yet been reached’’. Recently, This paper focuses on the blue-spotted maskray, Last et al. [24] described three new species (N. australiae, previously Neotrygon kuhlii (Mu¨ ller and Henle, 1841) N. caeruleopunctata, N. orientale) previously under [7], a stingray species that inhabits Indo-West Pacific N. kuhlii and resurrected a fourth one, N. varidens (Garman coral reefs, lagoons and slopes [8]. The blue-spotted 1885) [25]. Diagnostic morphological differences be- maskray is heavily exploited in Southeast Asia, but its tween the species were proposed but no in-depth catch rate and mortality rates are poorly known and its assessment of inter-specific against infra-specific diffe- population trends are unknown [9,10]. Authors have rences was included [24]. distinguished the ‘‘Java’’ (Java Sea) form of blue-spotted In the present paper, we compile all CO1 and maskray from the ‘‘Bali’’ (Kedonganan) form, based on cytochrome b gene sequences published thus far for the differences in size at birth and male size at maturity and blue-spotted maskray and we add new sequences from treated them as different species [9]. Molecular popula- samples collected in the western Indian Ocean and tion genetics offer the concepts and the practical tools for throughout the Indo-Malay archipelago, to construct a delineating populations, diagnosing closely related spe- robust mitochondrial phylogeny and establish an updated cies, and detecting cryptic species. Cryptic species are distribution of the clades previously uncovered in the defined as lineages with a substantial amount of genetic Coral Triangle region [14,15,17,19]. We assess whether distinctiveness and no detectable morphological diffe- the different clades, including those recently resurrected rences [11–13]. Ward et al. ([14]: 60–62) have noted that or erected as new species [24] correspond to evolutionary at the CO1 locus, ‘‘the D. kuhlii group showed considerable significant units that deserve the status of separate within species diversity . with four subgroups. One was species. the sole specimen from Australia (Queensland), one from the six specimens taken from Kedonganan fish market on Bali 2. Materials and methods (Indonesia), one from the five specimens from Muara Angke fish market at Jakarta, Java (Indonesia) and one from the 2.1. Ethics in sampling and information sharing three specimens from the Penghu Islands (Taiwan). Average distances among and within these four groups were 2.80% All specimens examined for the present study were and 0.18% respectively’’. Subsequent genetic studies in the independently captured by commercial fishers prior to genus Neotrygon have focused on its phylogeny [15–17], being sub-sampled for DNA. Some of the sampling P. Borsa et al. / C. R. Biologies 339 (2016) 417–426 419 Fig. 1. Sampling sites of blue-spotted maskrays, Neotrygon spp. previously under Neotrygon kuhlii, including new samples from present study, samples from the literature, and additional haplotypes from BOLD, Cryobank and GenBank (details in Supplementary Table S1).
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