Diversity and population genetic structure of Octopus hubbsorum in the Mexican Pacific inferred from mitochondrial DNA sequences
José de Jesús Dueñas-Romero A , Jasmín Granados-Amores B , Deivis Samuel Palacios-Salgado B , José Francisco Domínguez-Contreras C , Juan Ramón Flores-Ortega B and Francisco Javier García-Rodríguez C DA Programa de Doctorado en Ciencias Biológico Agropecuarias, Universidad Autónoma de Nayarit, Km. 9 Tepic-Compostela. 63780 Xalisco, Nayarit, México.
B Escuela Nacional de Ingeniería Pesquera, Universidad Autónoma de Nayarit (ENIP-UAN), Apartado Postal 10, C.P. 63740 San Blas, Nayarit, México.
C Instituto Politécnico Nacional-Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Avenue. IPN S/N, Col. Playa Palo de Santa Rita, CP 23096 La Paz, B.C.S., México.
D Corresponding author. Email: fjgarciar@ipn.mx
Marine and Freshwater Research 72(1) 35-43 https://doi.org/10.1071/MF19382
Submitted: 6 December 2019 Accepted: 3 May 2020 Published: 23 May 2020
Abstract
Octopus hubbsorum is the most commonly captured species of octopus on the western coast of Mexico. Despite the commercial importance of this species, management information remains scarce. We determined the genetic diversity and population genetic structure of O. hubbsorum by using mtDNA sequences (COI and ND5). The population structure was not supported by AMOVA or a spatial clustering model. Furthermore, an isolation by distance model did not explain our data. Three haplogroups were detected using a Bayesian assignment; however, the distribution of these haplogroups did not differ among the sampling sites. Our results indicated historical processes of a sudden population expansion, as has been reported for other species in the study region as consequence of climatic changes. However, this expansion did not affect the distribution of the mitochondrial lineages analysed in the study. The weak population genetic structure in O. hubbsorum associated with the life history of the species can explain our results. We suggest that to expand knowledge regarding the genetic structure and population dynamics of O. hubbsorum throughout its range, markers such as microsatellites or single-nucleotide polymorphisms (SNPs) are needed. Thus, on the basis of the information available, the studied population should be assumed to have a weak genetic structure.
Additional keywords: cephalopods, genetics, molluscs, phylogeography.
References
Alejo-Plata, M. C., and Herrero-Alejo, S. (2014). First description of eggs and paralarvae of green octopus Octopus hubbsorum (cephalopoda: Octopodidae) under laboratory conditions. American Malacological Bulletin 32, 132–139.| First description of eggs and paralarvae of green octopus Octopus hubbsorum (cephalopoda: Octopodidae) under laboratory conditions.Crossref | GoogleScholarGoogle Scholar |
Avise, J. C. (2000). ‘Phylogeography: the History and Formation of Species.’ (Harvard University Press: Cambridge, MA, USA.)
Barry, P. D., Tamone, S. L., and Tallmon, D. A. (2013). A complex pattern of population structure in the North Pacific giant octopus Enteroctopus dofleini (Wülker, 1910). The Journal of Molluscan Studies 79, 133–138.
| A complex pattern of population structure in the North Pacific giant octopus Enteroctopus dofleini (Wülker, 1910).Crossref | GoogleScholarGoogle Scholar |
Bohonak, A. J. (2002). IBD (isolation by distance): a program for analyses of isolation by distance. The Journal of Heredity 93, 153–154.
| IBD (isolation by distance): a program for analyses of isolation by distance.Crossref | GoogleScholarGoogle Scholar | 12140277PubMed |
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M. A., Rambaut, A., and Drummond, A. J. (2014). BEAST: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
| BEAST: a software platform for Bayesian evolutionary analysis.Crossref | GoogleScholarGoogle Scholar | 24722319PubMed |
Bravo-Olivas, M. L. (2008). Aspectos reproductivos del pulpo Octopus hubbsorum Berry, 1953 en el Parque Nacional ‘Bahía de Loreto’, Golfo de California. M.Sc. Thesis, Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, La Paz, Mexico.
Castillo-Olguín, E., Uribe-Alcocer, M., and Diaz-Jaimes, P. (2012). Assessment of the population genetic structure of Sphyrna lewini to identify conservation units in the Mexican Pacific. Ciencias Marinas 38, 635–652.
| Assessment of the population genetic structure of Sphyrna lewini to identify conservation units in the Mexican Pacific.Crossref | GoogleScholarGoogle Scholar |
Cheng, L., Connor, T. T., Sirén, J., Aanensen, D. M., and Corander, J. (2013). Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Molecular Biology and Evolution 30, 1224–1228.
| Hierarchical and spatially explicit clustering of DNA sequences with BAPS software.Crossref | GoogleScholarGoogle Scholar | 23408797PubMed |
Corander, J., Cheng, L., Marttinen, P., Sirén, J., and Tang, J. (2012). BAPS: Bayesian analysis of population structure (version 6.0). Available at http://www.helsinki.fi/bsg/software/BAPS [verified 15 January 2019].
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 22847109PubMed |
Diario Oficial de la Federación (2017). ACUERDO por el que se modifica el similar por el que se establece la veda temporal y tallas mínimas de captura para la pesca de las especies de pulpo en Bahía de los Ángeles, Baja California, publicado el 1 de junio de 2016, para considerar como zona de veda la Reserva de la Biosfera Bahía de los Ángeles, Canales de Ballenas y de Salsipuedes, respecto del pulpo café (Octopus bimaculatus) y pulpo verde (Octopus hubbsorum). Available at http://www.dof.gob.mx/nota_detalle.php?codigo=5503748&fecha=07/11/2017 [verified 06 October 2019].
Domínguez-Contreras, J. F. (2015). Distribución actual y conectividad genética de poblaciones de pulpo en el noroeste de México. Ph.D. Thesis, Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, La Paz, Mexico.
Domínguez-Contreras, J. F., Ceballos-Vázquez, B. P., Hochberg, F. G., and Arellano-Martínez, M. (2013). A new record in a well-established population of Octopus hubbsorum (Cephalopoda: Octopodidae) expands its known geographic distribution range and maximum size. American Malacological Bulletin 31, 95–99.
| A new record in a well-established population of Octopus hubbsorum (Cephalopoda: Octopodidae) expands its known geographic distribution range and maximum size.Crossref | GoogleScholarGoogle Scholar |
Domínguez-Contreras, J. F., Munguia-Vega, A., Ceballos-Vázquez, B. P., Arellano-Martínez, M., García-Rodríguez, F. J., Culver, M., and Reyes-Bonilla, H. (2018). Life histories predict genetic diversity and population structure within three species of octopus targeted by small-scale fisheries in Northwest Mexico. PeerJ 6, e4295.
| Life histories predict genetic diversity and population structure within three species of octopus targeted by small-scale fisheries in Northwest Mexico.Crossref | GoogleScholarGoogle Scholar | 29472993PubMed |
Excoffier, L., and Lischer, H. (2011). ‘Arlequin Ver. 3.5. An Integrated Software Package for Populations Genetics Data Analysis.’ (Swiss Institute of Bioinformatics: Bern, Switzerland.)
Fadhlaoui-Zid, K., Knittweis, L., Aurelle, D., Nafkha, Ch., Ezzeddine, S., Fiorentino, F., Ghmati, H., Ceriola, L., Jarboui, O., and Maltagliati, F. (2012). Genetic structure of Octopus vulgaris (Cephalopoda, Octopodidae) in the central Mediterranean Sea inferred from mitochondrial COIII gene. Comptes Rendus Biologies 335, 625–636.
| Genetic structure of Octopus vulgaris (Cephalopoda, Octopodidae) in the central Mediterranean Sea inferred from mitochondrial COIII gene.Crossref | GoogleScholarGoogle Scholar | 23199630PubMed |
FAO (2016). ‘The State of World Fisheries and Aquaculture. Contributing to Food Security and Nutrition for All.’ (FAO: Rome, Italy.)
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 7881515PubMed |
Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth and background selection. Genetics 147, 915–925.
| 9335623PubMed |
García-Rodríguez, F. J., Perez-Enriquez, R., Medina-Espinoza, A., and Vega-Velázquez, A. (2017). Genetic variability and historic stability of the California spiny lobster Panulirus interruptus in the Gulf of California. Fisheries Research 185, 130–136.
| Genetic variability and historic stability of the California spiny lobster Panulirus interruptus in the Gulf of California.Crossref | GoogleScholarGoogle Scholar |
Grant, W. S., and Cheng, W. (2012). Incorporating deep and shallow components of genetic structure into the management of Alaskan red king crab. Evolutionary Applications 5, 820–837.
| Incorporating deep and shallow components of genetic structure into the management of Alaskan red king crab.Crossref | GoogleScholarGoogle Scholar | 23346227PubMed |
Guerra, Á., Roura, Á., González, Á. F., Pascual, S., Cherel, Y., and Pérez-Losada, M. (2010). Morphological and genetic evidence that Octopus vulgaris Cuvier, 1797 inhabits Amsterdam and Saint Paul Islands (southern Indian Ocean). ICES Journal of Marine Science 67, 1401–1407.
| Morphological and genetic evidence that Octopus vulgaris Cuvier, 1797 inhabits Amsterdam and Saint Paul Islands (southern Indian Ocean).Crossref | GoogleScholarGoogle Scholar |
Hope, A. C. A. (1968). A simplified Monte Carlo significance test procedure. Journal of the Royal Statistical Society. Series B. Methodological 30, 582–598.
| A simplified Monte Carlo significance test procedure.Crossref | GoogleScholarGoogle Scholar |
Jereb, P., Roper, C. F. E., Norman, M. D., and Finn, J. K. (2016). ‘Cephalopods of the World: an Annotated and Illustrated Catalogue of Cephalopod Species Known to Date.’ (FAO: Rome, Italy.)
Kang, J. H., Park, J. Y., and Choi, T. J. (2012). Genetic differentiation of octopuses from different habitats near the Korean peninsula and eastern China based on analysis of the mDNA cytochrome C oxidase 1 gene. Genetics and Molecular Research 11, 3988–3997.
| Genetic differentiation of octopuses from different habitats near the Korean peninsula and eastern China based on analysis of the mDNA cytochrome C oxidase 1 gene.Crossref | GoogleScholarGoogle Scholar | 23212336PubMed |
Kogura, Y., Seeb, J. E., and Azuma, N. (2011). The genetic population structure of lacustrine sockeye salmon, Oncorhynchus nerka, in Japan as the endangered species. Environmental Biology of Fishes 92, 539–550.
| The genetic population structure of lacustrine sockeye salmon, Oncorhynchus nerka, in Japan as the endangered species.Crossref | GoogleScholarGoogle Scholar |
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |
Lecomte, F., Grant, S. W., Dodson, J. J., Rodriguez-Sanchez, R., and Bowens, W. B. (2004). Living with uncertainty: genetic imprints of climate shifts in East Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax). Molecular Ecology 13, 2169–2182.
| Living with uncertainty: genetic imprints of climate shifts in East Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax).Crossref | GoogleScholarGoogle Scholar | 15245392PubMed |
León-Guzmán, S. S., and Alejo-Plata, M. C. (2015). Octopus hubbsorum el pulpo verde de Oaxaca. Temas de Ciencia y Tecnología 19, 61–64.
López-Uriarte, E., and Ríos-Jara, E. (2009). Reproductive biology of Octopus hubbsorum (Mollusca: Cephalopoda) along the central Mexican Pacific coast. Bulletin of Marine Science 84, 109–121.
López-Uriarte, E., Ríos-Jara, E., and Pérez-Peña, M. (2005). Range extension for Octopus hubbsorum (Mollusca: Octopodidae) in the Mexican Pacific. Bulletin of Marine Science 77, 171–175.
Lü, Z. M., Liu, L. Q., Li, H., Wu, C. W., and Zhang, J. S. (2013). Deep phylogeographic break among Octopus variabilis populations in China: evidence from mitochondrial and nuclear DNA analyses. Biochemical Systematics and Ecology 51, 224–231.
| Deep phylogeographic break among Octopus variabilis populations in China: evidence from mitochondrial and nuclear DNA analyses.Crossref | GoogleScholarGoogle Scholar |
Makhawi, A. M., Liu, X.-B., and Yang, S.-R. (2013). Genetic variations of ND5 gene of mtDNA in populations of Anopheles sinensis (Diptera: Culicidae) malaria vector in China. Parasites & Vectors 6, 290.
| Genetic variations of ND5 gene of mtDNA in populations of Anopheles sinensis (Diptera: Culicidae) malaria vector in China.Crossref | GoogleScholarGoogle Scholar |
Marinone, S. G. (2012). Seasonal surface connectivity in the Gulf of California. Estuarine, Coastal and Shelf Science 100, 133–141.
| Seasonal surface connectivity in the Gulf of California.Crossref | GoogleScholarGoogle Scholar |
Marinone, S. G., Lavín, M. F., and Parés-Sierra, A. (2011). A quantitative characterization of the seasonal Lagrangian circulation of the Gulf of California from a three dimensional numerical model. Continental Shelf Research 31, 1420–1426.
| A quantitative characterization of the seasonal Lagrangian circulation of the Gulf of California from a three dimensional numerical model.Crossref | GoogleScholarGoogle Scholar |
Melis, R., Vacca, L., Cuccu, D., Mereu, M., Cau, A., Follesa, M. C., and Cannas, R. (2018). Genetic population structure and phylogeny of the common octopus Octopus vulgaris Cuvier, 1797 in the western Mediterranean Sea through nuclear and mitochondrial markers. Hydrobiologia 807, 277–296.
| Genetic population structure and phylogeny of the common octopus Octopus vulgaris Cuvier, 1797 in the western Mediterranean Sea through nuclear and mitochondrial markers.Crossref | GoogleScholarGoogle Scholar |
Muhammad, F., Liu, L., Lu, Z. M., Gong, L., Du, X., Shafi, M., Waryani, B., and Kaleri, H. A. (2018). Genetic diversity of Octopus minor (Sasaki, 1920) inferred by mitochondrial NADH dehydrogenase subunit 2 gene. The Journal of Animal and Plant Sciences 28, 1364–1371.
Muhammad, F., Chen, W., Liu, L., Gong, L., Xun, D., Shafi, M., and Lü, Z. (2019). Genetic structure of Amphioctopus fangsiao (Mollusca, Cephalopoda) in Chinese waters inferred from variation in three mtDNA genes (ATPase 6, ND2, and ND5). Hydrobiologia 838, 111–119.
| Genetic structure of Amphioctopus fangsiao (Mollusca, Cephalopoda) in Chinese waters inferred from variation in three mtDNA genes (ATPase 6, ND2, and ND5).Crossref | GoogleScholarGoogle Scholar |
Palumbi, S. R. (2003). Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications 13, 146–158.
| Population genetics, demographic connectivity, and the design of marine reserves.Crossref | GoogleScholarGoogle Scholar |
Pardo-Gandarillas, M. C., Ibáñez, C. M., Yamashiro, C., Méndez, M. A., and Poulin, E. (2018). Demographic inference and genetic diversity of Octopus mimus (Cephalopoda: Octopodidae) throughout the Humboldt Current System. Hydrobiologia 808, 125–135.
| Demographic inference and genetic diversity of Octopus mimus (Cephalopoda: Octopodidae) throughout the Humboldt Current System.Crossref | GoogleScholarGoogle Scholar |
Peguero-Icaza, M., Sánchez-Velasco, L., Lavin, M. F., Marinone, S. G., and Beier, E. (2011). Seasonal changes in connectivity routes among larval fish assemblages in a semi-enclosed sea (Gulf of California). Journal of Plankton Research 33, 517–533.
| Seasonal changes in connectivity routes among larval fish assemblages in a semi-enclosed sea (Gulf of California).Crossref | GoogleScholarGoogle Scholar |
Pliego-Cárdenas, R., García-Domínguez, F. A., Ceballos-Vázquez, B. P., Villalejo-Fuerte, M., and Arellano-Martínez, M. (2011). Reproductive aspects of Octopus hubbsorum (Cephalopoda, Octopodidae) from Espíritu Santo Island, southern Gulf of California, México. Ciencias Marinas 37, 23–32.
| Reproductive aspects of Octopus hubbsorum (Cephalopoda, Octopodidae) from Espíritu Santo Island, southern Gulf of California, México.Crossref | GoogleScholarGoogle Scholar |
Ramos-Onsins, S. E., and Rozas, J. (2002). Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 2092–2100.
| Statistical properties of new neutrality tests against population growth.Crossref | GoogleScholarGoogle Scholar | 12446801PubMed |
Reding, D. M., Carter, C. E., Hiller, T. L., and Clark, W. R. (2013). Using population genetics for management of bobcats in Oregon. Wildlife Society Bulletin 37, 342–351.
| Using population genetics for management of bobcats in Oregon.Crossref | GoogleScholarGoogle Scholar |
Rodríguez-Tapia, M. A., Chávez-Ríos, K., García-Ibañez, S., and Ojendiz-Mancilla, J. (2013). Ciclo reproductivo y morfometría de Octopus hubbsorum en Acapulco, Guerrero, México. Medio Ambiente y Recursos Naturales 1, 423–427.
Rogers, A. R., and Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.
| 1316531PubMed |
Rousset, F. (1997). Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228.
| 9093870PubMed |
Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., and Sánchez-Gracia, A. (2017). DnaSP v6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution 34, 3299–3302.
| DnaSP v6: DNA sequence polymorphism analysis of large datasets.Crossref | GoogleScholarGoogle Scholar | 29029172PubMed |
RStudio Team (2019). RStudio: integrated development for R. RStudio, Inc., Boston, MA, USA. Available at http://www.rstudio.com/.
Saccone, C., de Giorgi, C., Gissi, C., Pesole, G., and Reyes, A. (1999). Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system. Gene 238, 195–209.
| Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system.Crossref | GoogleScholarGoogle Scholar | 10570997PubMed |
Sánchez-Velasco, L., Lavin, M. F., Peguero-Icaza, M., León-Chávez, C. A., Contreras-Catala, F., Marinone, S. G., Gutiérrez-Palacios, I. V., and Godínez, V. M. (2009). Seasonal changes in larval fish assemblages in a semi-closed sea (Gulf of California). Continental Shelf Research 29, 1697–1710.
| Seasonal changes in larval fish assemblages in a semi-closed sea (Gulf of California).Crossref | GoogleScholarGoogle Scholar |
Sánchez-Velasco, L., Lavin, M. F., Jiménez-Rosenberg, S. P. A., Godínez, V. M., Santamaría-del-Angel, E., and Hernández-Becerril, D. U. (2013). Three-dimensional distribution of fish larvae in a cyclonic Eddy in the Gulf of California during the summer. Deep-sea Research. Part I, Oceanographic Research Papers 75, 39–51.
| Three-dimensional distribution of fish larvae in a cyclonic Eddy in the Gulf of California during the summer.Crossref | GoogleScholarGoogle Scholar |
SIAP (2017). Producción pesquera de pulpo 2015. Servicio de Información Agroalimentaria y Pesquera. Available at http://pesca.siap.gob.mx/produccion/rep_mensual_esp_opc_gobmx.php?tipo=0&anioRep=2017&entidadFed=130500 [verified 6 October 2019].
SIAP (2018). Producción pesquera de pulpo 2015. Servicio de Información Agroalimentaria y Pesquera. Available at http://pesca.siap.gob.mx/produccion/rep_mensual_esp_opc_gobmx.php?tipo=0&anioRep=2018&entidadFed=130500 [verified 6 October 2019].
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
| 2513255PubMed |
Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., and Rozen, S. G. (2012). Primer3: new capabilities and interfaces. Nucleic Acids Research 40, e115.
| Primer3: new capabilities and interfaces.Crossref | GoogleScholarGoogle Scholar | 22730293PubMed |
Xia, X. (2017). DAMBE6: New tools for microbial genomics, phylogenetics and molecular evolution. The Journal of Heredity 108, 431–437.
| DAMBE6: New tools for microbial genomics, phylogenetics and molecular evolution.Crossref | GoogleScholarGoogle Scholar | 28379490PubMed |
Yu, J.-N., Azuma, N., and Abe, S. (2012). Genetic differentiation between collections of hatchery and wild masu salmon (Oncorhynchus masou) inferred from mitochondrial and microsatellite DNA analyses. Environmental Biology of Fishes 94, 259–271.
| Genetic differentiation between collections of hatchery and wild masu salmon (Oncorhynchus masou) inferred from mitochondrial and microsatellite DNA analyses.Crossref | GoogleScholarGoogle Scholar |