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Population Genetics of the Jumbo Squid Dosidicus Gigas (Cephalopoda

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Population Genetics of the Jumbo Squid Dosidicus Gigas (Cephalopoda Fisheries Research 175 (2016) 1–9 Contents lists available at ScienceDirect Fisheries Research j ournal homepage: www.elsevier.com/locate/fishres Population genetics of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) in the northern Humboldt Current system based on mitochondrial and microsatellite DNA markers a a b c Gustavo Sanchez , Satoshi Tomano , Carmen Yamashiro , Ricardo Fujita , d e a,∗ Toshie Wakabayashi , Mitsuo Sakai , Tetsuya Umino a Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima, Hiroshima 739-8528, Japan b Unidad de Investigación en Invertebrados Marinos, Instituto del Mar del Perú, Esquina Gamarra y General Valle s/n, Chucuito, Callao, Peru c Centro de Genética y Biología Molecular, Facultad de Medicina Humana de la Universidad de San Martín de Porres, Lima, Peru d Department of Fisheries Science and Technology, National Fisheries University, Shimonoseki, Yamaguchi 759-6595, Japan e Tohoku National Fisheries Research Institute, Hachinohe, Aomori 031-0841, Japan a r t i c l e i n f o a b s t r a c t Article history: Jumbo squid, Dosidicus gigas, is commercially important species in the Eastern Pacific Ocean, principally Received 15 June 2015 in the Northern Humboldt Current System where is notably abundant. In this area, jumbo squid display Received in revised form 24 October 2015 difference in density at geographical level, in size of mature individuals and inter-annual demographic Accepted 4 November 2015 fluctuation. Thereby, a population genetics study of jumbo squid in this location is needed especially for Available online 21 November 2015 fisheries management. This study evaluated the population genetic of this squid (n = 120) based on novel microsatellite loci and 675 bp of the mtDNA ND2 divided into two groups according to the Geographical Keywords: density and Size at maturity. Our results at nuclear loci showed an overall low genetic diversity and no Population genetics signatures of genetic differentiation of any group. At mtDNA loci level, low but significant genetic differ- Jumbo squid Microsatellite entiation were detected between Small (n = 33) and Large (n = 39) populations. The low genetic diversity mtDNA ND2 is more likely explained by a historical demographic expansion whereas the contradictory results of Northern Humboldt Current system population structure may be due to the low number of microsatellite loci in HWE, different maternal history of this species or the different influence of genetic drift on mitochondrial and nuclear genes. Fur- thermore, demographic history analysis suggested that jumbo squid population went through a period of pure demographic expansion over the last 50,000 years ago. This study provides results of combined nuclear and mtDNA molecular markers that was never reported before and may represent a valuable information for the monitoring of the population genetic of this species. © 2015 Elsevier B.V. All rights reserved. ◦ 1. Introduction 2001). In addition, a recent extension to 60 N during unusual warm surface waters in 2004 has been reported (Cosgrove, 2005; Wing, The ommastrephid squid Dosidicus gigas (d’Orbigny, 1835) also 2006). Sub-populations of this species throughout its geographical known as the jumbo or Humboldt squid is one of the largest and distribution have been previously identified based on the mature most abundant nektonic squid in the epipelagic zone of the world’s individual sizes determined as dorsal mantle length (Nigmatullin oceans (Roper et al., 1984). Jumbo squid is endemic to the East- et al., 2001). Small individual-size population is found predomi- ern Pacific Ocean and its distribution commonly stretches from nantly in equatorial waters, the Medium individual-size population ◦ ◦ ◦ ◦ 30 N to 25 S and occasionally from 40 N to 47 S (Nigmatullin et al., along the species distribution, and the Large individual-size popula- tion in the northern and southern peripheries of the total range. This size variations is explained by two different hypotheses; the first suggests the presence of genetically distinct populations (Nesis, ∗ Corresponding author. Fax: +81 824 24 7944. 1983), whereas the second and more plausible suggests the pres- E-mail addresses: [email protected] ence of these populations as a response to environmental variation (G. Sanchez), [email protected] (S. Tomano), and food availability (Keyl et al., 2008; Sandoval-Castellanos et al., [email protected] (C. Yamashiro), [email protected] 2009; Staaf et al., 2010; Tafur et al., 2010). (R. Fujita), twakaba@fish-u.ac.jp (T. Wakabayashi), [email protected] (M. Sakai), [email protected] (T. Umino). http://dx.doi.org/10.1016/j.fishres.2015.11.005 0165-7836/© 2015 Elsevier B.V. All rights reserved. 2 G. Sanchez et al. / Fisheries Research 175 (2016) 1–9 Landing of jumbo squid occurs mainly within the exclusive catch density at geographical level and size of mature individuals economic zones (EEZs) of Peru, Chile, and Mexico with a com- (DML). Additionally, an evaluation of jumbo squid in an extensive bined annual production of approximately 0.66–0.75 million tons area of the Humboldt Current System was analyzed with sequences between the years 2008 and 2012 (FAO, 2014). Particularly, the from the Chilean waters. marine ecosystem off Peru, i.e., the northern Humboldt Current System (HCS), is one of the most productive areas with remark- 2. Materials and methods able fisheries production compared to currents of the Pacific and Atlantic Oceans (Bakun and Weeks, 2008). Here, jumbo squid is 2.1. Sample collection and DNA extraction highly abundant and supports one of the world’s most impor- tant invertebrate fisheries (Roper et al., 1984; Taipe et al., 2001; A total of 120 individuals of jumbo squid were collected in Yamashiro et al, 1998). During 2012, overall global production of ◦ Peruvian waters at 4–16 S by the research vessel R/V Kaiyo Maru jumbo squid in Peru was estimated at >0.49 million tons, which from December 16th 2011 to January 19th 2012 (Fig. 1). The dorsal represents more than 50% of its global production in all of the fish- mantle length (DML) of each individual was measured and histolog- eries areas within the EEZ and international offshore waters(FAO, ical techniques were performed to determine the maturity stage. 2014). The main fishing grounds for this squid in the Peruvian ◦ Immediately after measure, approximately 2 cm of muscular tissue EEZ are situated between 2 and 10 S, whereas fishing in interna- ◦ from arm was isolated from each individual and stored in 99.5% tional waters off Peru are situated between 3 and 18 S (Waluda ethanol for molecular analysis. Genomic DNA was extracted from and Rodhouse, 2005). The international fleet mainly consists of a small piece of tissue using TNES-urea buffer (Asahida et al., 1996) vessels with Asian flag (Korea, China, and Japan), which landed followed by the standard phenol-chloroform isolation. 0.28 million tons combined in the Pacific South East in 2012 The analysis was performed on the basis of two different groups, (FAO, 2014). However, production of this species may be sub- herein named as Geographical density (catch density at geographi- jected to high inter-annual variability. In fact, high variability in cal level) and Size at maturity group. For the first group, individuals catch density of jumbo squid was reported during 1991–1999 at were pooled according to the geographical origin of the sam- geographical level along Peruvian coast, with high concentrations ◦ ◦ ◦ ◦ ples and named as North (4–10 S) and Central–South (11–16 S) from 3 24 –9 S to low-medium densities observed in the south populations. For the second group, individuals were pooled into (Taipe et al., 2001). Additionally, year to year fluctuations in catches Small, Medium, and Large population according to the DML at occurred in Peruvian waters (Rodhouse, 2001; Waluda et al., 2006) maturity data following Nigmatullin et al. (2001) with a slight with a remarkable high abundance after a strong El Nino˜ event in modification to exclude overlapping between populations. Consid- 1997–1998. Therefore, this fluctuation is possibly influenced by cli- ering males and females, the modification was as follows: Small matic variations such as the variable El Nino˜ Southern Oscillation population (13–26 cm and 14–34 cm, respectively), medium popu- (ENSO) events in the upwelling system off Peru (Rodhouse, 2001) lation (27–42 cm and 35–60 cm, respectively), and large population and by of the overexploitation (Xavier et al., 2014). (43–50 cm and 61–120 cm, respectively). Squid have natural ability to recover from low biomass—level that may occur during unfavorable conditions, nonetheless a strong 2.2. Microsatellite development fishing pressure during such periods could negatively affect the recovery process and, consequently, their fishing stocks (Arkhipkin Pooled Genomic DNA from the arm tissue of seven individ- et al., 2015). Thus, considering the importance that jumbo squid uals of jumbo squid was digested with Sau3AI. DNA fragments represents for global cephalopod catch, it is essential to under- between 500 and 1000 bp were selected from agarose gel using a stand the drivers affecting the spatial and temporal variations, QIA-quick Gel Extraction Kit (Qiagen, Germany). Around 300 ng of density and further how these yearly fluctuations affect the popu- the fragments was ligated into a pUC19 vector according to manu- lation of this species. Most commonly used methods in the recent facterıs´ protocol (Takara
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