Abstract
Deep-sea shrimps of the species Plesionika acanthonotus (Smith, 1882) and P. holthuisi Crosnier & Forest, 1968 are morphologically similar and exhibit overlapping amphi-Atlantic distributions. In the literature, through morphological studies, there are reports of doubts about the validity of P. holthuisi and some authors believe that the eastern and western Atlantic populations of P. acanthonothus could represent two distinct species. The objective of the present study was to use molecular data to elucidate the taxonomic status of the two populations of P. acanthonothus. DNA sequences of two mitochondrial genes (16S rDNA and Cytochrome Oxidase subunit I) and a nuclear gene (Histone 3) were obtained for both species and for both populations of P. acanthonotus. The sequences were also obtained from Genbank for comparison. The trees (separate and multi-locus/partitioned genes) were generated by Bayesian Inference analyzes, and genetic divergence (Kimura-2-parameters) was also calculated. All specimens that had their DNA sequenced were examined morphologically to confirm their identification; morphological variations were noted. The genetic data showed that Plesionika holthuisi is closely related to P. acanthonotus, but clearly separated, indicating that P. holthuisi is a valid species. In the multi-locus analysis, the P. acanthonothus specimens were divided into two clades, one with the eastern Atlantic specimens and another with the western Atlantic specimens. However, this genetic separation was considered to be a population structuring for three reasons: (1) the genetic divergences of the two mitochondrial genes between these two groups (eastern Atlantic X western Atlantic) were smaller than the interspecific divergence for Plesionika; (2) the P. acanthonothus sequences of the Histone 3 gene showed no genetic variation; (3) in the analyzed individuals, no valid morphological character was found to support this separation. Thus, the conclusion of this study is that P. holthuisi probably is a valid species and P. acanthonothus presents two populations with mitochondrial divergences that could be in the process of speciation, but which currently represent only one species.
References
Ahamed, F., Cardoso, I., Ahmed, O., Hossain, Y. & Ohtomi, J. (2017) An overview of the genus Plesionika Bate, 1888 (Decapoda, Caridea, Pandalidae) in Asian waters. Zootaxa, 4221 (5), 575–593.
https://doi.org/10.11646/zootaxa.4221.5.6
Aznar-Cormano, L., Brisset, J., Chan, T.Y., Corbari, L., Puillandre, N., Utge, J., Zbinden, M., Zuccon, D. & Samadi, S. (2015) An improved taxonomic sampling is a necessary but not sufficient condition for resolving inter-families relationships in Caridean decapods. Genetica, 143 (2), 195–205.
https://doi.org/10.1007/s10709-014-9807-0
Besbes, N., Jérôme, M., Bergé, J. & Sadok, S. (2015) Authenticating the origin of different shrimp products on the Tunisian markets by PCR/RFLP method. African Journal of Biotechnology, 14 (29), 2273–2281.
Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2006) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22 (3), 148–155.
https://doi.org/10.1016/j.tree.2006.11.004
Bourdillon-Casanova, L. (1960) Le méroplancton du Golfe de Marseille: Les larves de crustacés décapodes. Recueil des Traveaux du Station Marine d’Endoume, 30 (18), 1–286.
Bracken, H.D., De Grave, S. & Felder, D.L. (2009) Phylogeny of the infraorder Caridea based on mitochondrial and nuclear genes (Crustacea: Decapoda). In: Martin, J.W., Crandall, K.A. & Felder, D.L. (Eds.), Decapod Crustacean Phylogenetics. CRC Press Taylor & Francis Group. Crustacean Issues, 18, 281–305.
https://doi.org/10.1201/9781420092592-c14
Bracken, H.D., De Grave, S., Toon, A., Felder, D.L. & Crandall, K.A. (2010) Phylogenetic position, systematic status, and divergence time of the Procarididea (Crustacea: Decapoda). Zoologica Scripta, 39, 198–212.
https://doi.org/10.1111/j.1463-6409.2009.00410.x
Campisi, S., Mura, M. & Cau, A. (1998) Biological aspects of Plesionika antigai (Zariquiey Alvarez, 1955) (Crustacea: Decapoda: Pandalidae) in central-western Mediterranean. Journal of Natural History, 32, 1453–1462.
https://doi.org/10.1080/00222939800770991
Cardoso, I.A. (2009) Report on some Plesionika Bate, 1888 and first record of Stylopandalus Coutiére, 1905 (Caridea, Pandalidae) from Brazilian waters. Zootaxa, 2120, 53–68.
Cardoso, I.A. (2010) Redescription of the sibling species Plesionika acanthonotus (Smith, 1882) and Plesionika holthuisi Crosnier & Forest, 1968 (Caridea, Pandalidae). Atlântica, 32 (2), 22–135.
https://doi.org/10.5088/atl.2010.32.2.221
Cardoso, I.A. (2011a) Three species of the genus Plesionika Bate, 1888 (Caridea: Pandalidae) reported for the first time in the southwestern Atlantic. Cahiers de Biologie Marine, 52, 131–146.
Cardoso, I.A. (2011b) New species of Plesionika Bate, 1888 (Crustacea, Decapoda, Pandalidae) from Southwestern Atlantic. Zootaxa, 3089, 51–59.
Chakraborty, R.D, Chan, T.Y., Maheswarudu, G., Kuberan, G., Purushothaman, P. & Chang, S.C. (2015) Plesionika quasigrandis Chace, 1985 (Decapoda, Caridea, Pandalidae) from Southwestern India. Crustaceana, 88 (7–8), 923–930.
https://doi.org/10.1163/15685403-00003451
Chan, T. (2004) The Plesionika rostricrescentis (Bate, 1888) and P. lophotes groups of Plesionika Bate, 1888, with descriptions of five new species (Crustacea, Decapoda, Pandalidae). In: Marshall, B. & Richer de Forges, B. (Eds.), Tropical Deep-Sea Benthos. Vol. 23. Memoires of the Museum National d´Histoire Naturelle, Paris, 191, pp. 293–318.
Chan, T. & Chuang, C. (2002) A new shrimp species of Plesionika Bate, 1888 with high basal rostral crest (Crustacea: Decapoda: Pandalidae) from Taiwan. Proceedings of the Biological Society of Washington, 115 (3), 611–615.
Chan, T. & Crosnier, A. (1991) Crustacea Decapoda: Studies of the Plesionika narval (Fabricius, 1787) group (Pandalidae) with descriptions of six new species. In: Crosnier, A. (Ed.), Resultáts des Campagnes MUSORSTOM. Vol. 9. Memoires of the Museum National d´Histoire Naturelle, Paris, 152, pp. 413–461.
Chan, T. & Crosnier, A. (1997) Crustacea Decapoda: deep-sea shrimps of the genus Plesionika bate, 1888 (Pandalidae) from French Polynesia, with descriptions of five new species. In: Crosnier, A. (Ed.), Resultáts des Campagnes MUSORSTOM. Vol. 18. Memoires of the Museum National d´Histoire Naturelle, Paris, 176, pp. 187–234.
Chan, T. & Yu, P. (1991) Two similar species: Plesionika edwardsii (Brandt, 1851) and Plesionika crosnieri, new species (Crustacea: Decapoda: Pandalidae). Proceedings of the Biological Society of Washington, 104 (3), 545–555.
Company, J.B. & Sardá, F. (1998) Metabolic rates and energy content of deep-sea benthic decapod crustaceans in the Western Mediterranean Sea. Deep-Sea Research, Part I, 45, 1861–1880.
https://doi.org/10.1016/S0967-0637(98)00034-X
Crosnier, A. & Forest, J. (1968) Note préliminaire sur les carides recueillis par l’Ombango au large du plateau continental, du Gabon à l’Angola (Crustacea Decapoda Natantia). Bulletin du Museum National d´Histoire Naturelle, 39, 1123–1147.
Crosnier, A. & Forest, J. (1973) Les crevettes profondes de l’Atlantique oriental tropical. Faune Tropicale, 19, 1–409.
Cruz, N. & Fransen, C.H.J.M. (2004) Addition of three species of the genus Plesionika (Crustacea: Caridea: Pandalidae) to the known Atlantic marine fauna of Colombia. Zoologische Mededelingen, 78, 131–146.
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9 (8), 772.
https://doi.org/10.1038/nmeth.2109
De Grave, S., Pentcheff, N.D., Ahyong, S.T., Chan, T.Y., Crandall, K.A., Dworschak, P.C., Felder, D.L., Feldmann, R.M., Fransen, C.H.J.M., Goulding, L.Y.D., Lemaitre, R., Low, M.E.Y., Martin, J.W., Ng, P.K.L., Schweitzer, S.E., Tan, S., Tshudy, D.H. & Wetzer, R. (2009) A classification of living and fossil genera of Decapod Crustaceans. Raffles Bulletin of Zoology, 21, 1–109.
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29 (8), 1969–1973.
https://doi.org/10.1093/molbev/mss075
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797.
https://doi.org/10.1093/nar/gkh340
Fransen, C.H.J.M. (2006) Pandalidae (Crustacea: Decapoda) of the Sonne, Valdivia and Meteor Expeditions, 1977–1987, to the Red Sea and the Gulf of Aden. Senckenbergiana Maritima, 36 (1), 51–82.
https://doi.org/10.1007/BF03043702
Gusmão, J. & Sole-Cava, A.M. (2002) Um sistema de diagnóstico molecular para a identificação de espécies comerciais de camarões marinhos brasileiros. CIVA 2002: Comunicaciones y Foros de Discusión, 1, 754–764.
Hellberg, M.E. (2009) Gene flow and isolation among populations of marine animals. Annual Review of Ecology and Systematics, 40, 291–310.
https://doi.org/10.1146/annurev.ecolsys.110308.120223
Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.
https://doi.org/10.1093/bioinformatics/17.8.754
Kimura, N. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
https://doi.org/10.1007/BF01731581
Landeira, J.M., Chan, T.Y., Aguilar-Soto, N., Jiang, G.C. & Yang, C.H. (2014) Description of the decapodid stage of Plesionika narval (Fabricius, 1787) (Decapoda: Caridea: Pandalidae) identified by DNA barcoding. Journal of Crustacean Biology, 34 (3), 377–387.
https://doi.org/10.1163/1937240X-00002234
Mathews, L.M., Schubart, C.D., Neigel, J.E. & Felder, D.L. (2002) Genetic, ecological, and behavioral divergence between two sibling snapping shrimp species (Crustacea: Decapoda: Alpheus). Molecular Ecology, 11, 1427–1437.
Matzen da Silva, J., Creer, S., dos Santos, A., Costa, A., Cunha, M., Costa, F. & Carvalho, G. (2011) Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca). PlosOne, 6 (5), 1–15.
Matzen da Silva, J., dos Santos, A., Cunha, M., Costa, F., Creer, S. & Carvalho, G. (2013) Investigating the molecular systematic relationships amongst selected Plesionika (Decapoda: Pandalidae) from the Northeast Atlantic and Mediterranean Sea. Marine Ecology, 34, 15–170.
https://doi.org/10.1111/j.1439-0485.2012.00530.x
Mayr, E. (1963) Animal Species and Evolution. Harvard University Press, Cambridge.
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, 2010, 1–8.
https://doi.org/10.1109/GCE.2010.5676129
Moritz, C., Dowling, T.E. & Brown, W.M. (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annual Review of Ecology and Systematics, 18 (1), 269–292.
https://doi.org/10.1146/annurev.es.18.110187.001413
Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer. Version 1.6. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed August 2018)
Radulovici, A.E., Sainte-Marie, B., Dufresne, F. (2009) DNA barcoding of marine crustaceans from the Estuary and Gulf of St Lawrence: a regional-scale approach. Molecular Ecology Resources, 1 (Supplement), 181–7.
https://doi.org/10.1111/j.1755-0998.2009.02643.x
Rice, P., Longden, I. & Bleasby, A. (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends in Genetics, 16 (6), 276–277.
https://doi.org/10.1016/S0168-9525(00)02024-2
Schubart, C.D. & Huber, M.G.J. (2006) Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae). Bulletin Français de la Pêche et de la Pisciculture, 380–381, 1019–1028.
https://doi.org/10.1051/kmae:2006008
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
https://doi.org/10.1093/molbev/mst197
Teodoro, S.S.A., Terossi, M., Costa, R.C. & Mantelatto, F.L. (2015) Genetic homogeneity in the commercial pink shrimp Farfantepenaeus paulensis revealed by COI barcoding gene. Estuarine, Coastal and Shelf Science, 166, 124–130.
Tong, J.G., Chan, T.Y. & Chu, K.H. (2000) A preliminary phylogenetic analysis of Metapenaeopsis (Decapoda: Penaeidae) based on mitochondrial DNA sequences of selected species from the Indico-West Pacific. Journal of Crustacean Biology, 20, 541–549.
https://doi.org/10.1163/20021975-99990070
Vafidis, D., Chrissi-Yianna, P., Carbonell, A. & Company, J. (2005) A review of the biology and fisheries of the genus Plesionika Bate, 1888 (Decapoda, Caridea, Pandalidae) in European waters. Crustaceana, 78 (3), 335–352.
https://doi.org/10.1163/1568540054286592
Xia, X. (2013) DAMBE5: A comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution, 30 (7), 1–9.
https://doi.org/10.1093/molbev/mst064
Xia, X. & Lemey, P. (2009) Assessing substitution saturation with DAMBE. In: Lemey, P., Salemi, M. & Vandamme, A.M. (Eds.), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. 2nd edition, Cambridge University Press, Cambridge, pp. 615–630.
https://doi.org/10.1017/CBO9780511819049.022
Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1–7.
https://doi.org/10.1016/S1055-7903(02)00326-3
Zuccon, D., Brisset, J., Corbari, L., Puillandre, N., Utge, J. & Samadi, S. (2012) An optimized protocol for barcoding museum collections of decapod crustaceans: a case-study for a 10–40-years-old collection. Invertebrate Systematics, 26 (5–6), 592–600.