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Population genetic structure of jumbo squid

(Dosidicus gigas) evaluated by RAPD analysis
ARTICLE in FISHERIES RESEARCH JANUARY 2007
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Fisheries Research 83 (2007) 113118

Population genetic structure of jumbo squid (Dosidicus gigas)

evaluated by RAPD analysis
Edson Sandoval-Castellanos , Manuel Uribe-Alcocer, Pndaro Daz-Jaimes
Instituto de Ciencias del Mar y Limnologa, Universidad Nacional Autonoma de Mexico, Circuito Exterior de Ciudad Universitaria,
Insurgentes Sur 3000, Coyoacan, Mexico D.F. 04510, Mexico
Received 15 April 2006; received in revised form 19 September 2006; accepted 21 September 2006

Abstract
The jumbo squid (Dosidicus gigas) supports important fisheries, with the maximum landings being recorded in Mexico, Peru and Chile.
To evaluate genetic structure and to measure the impact of temporal variation, randomly amplified polymorphic DNA (RAPD) data were
generated and analysed from 210 samples from eight eastern Pacific sites and on two sample sets taken from the same location in consecutive years.
The temporal variation was shown to have no significant effect on genetic diversity. In addition, a genetic structure was detected which divided
the populations into northern and southern locations. There was marginal isolation by distance between populations. Like in other ommastrephids,
genetic structure is considered evidence of an adaptive radiation.
2006 Elsevier B.V. All rights reserved.
Keywords: Dosidicus gigas; Genetic structure; Jumbo squid; RAPDs

1. Introduction
With record landings over 700,000 t in 2004 (FAO, 2006) the
Dosidicus gigas fishery is the most important cephalopod fishery of the eastern Pacific (Taipe et al., 2001). It is an outstanding
representative of income for countries like Mexico, Peru and
Chile. However, the management of cephalopod fisheries suffers from difficulties derived from their short life cycles and the
lack of information the species (Caddy, 1983). To aid management, it is necessary to define the existing fishery stocks through
determination of genetically discrete populations (Carvalho and
Hauser, 1994; Ward, 2000).
The distribution of D. gigas is restricted to the eastern Pacific,
ranging from 3740 N to 4547 S and up to the 125140 W
along the equator (Nigmautllin et al., 2001). It reaches high
densities off the Peruvian coast in the southern hemisphere and
in the Gulf of California in the northern hemisphere (Taipe et
al., 2001). The northern hemisphere organisms migrate from
the Pacific into the Gulf of California during the winter/spring
seasons and return in summer/autumn. Spawning peaks have
been detected in summer and winter inside the Gulf of California

Corresponding author. Tel.: +52 55 56225842; fax: +52 55 56160748.

E-mail address: edsc30@yahoo.com.mx (E. Sandoval-Castellanos).

0165-7836/$ see front matter 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.fishres.2006.09.007

and nearby waters (Ehrhardt et al., 1986; Hernandez-Herrera et

al., 1996). The southern hemisphere organisms migrate from two
spawning grounds (38 and 1217 S) to the south and east and
to the north and east approaching the Peruvian coast (Yamashiro
et al., 1997; Taipe et al., 2001).
Spawning occurs mainly in southern spring and summer
(Taipe et al., 2001). There are at least three different cohorts,
which arise from different spawning periods with different maturation and growth rates (Ehrhardt et al., 1986; Markaida et al.,
2004, 2005; Arguelles et al., 2001; Taipe et al., 2001; Tafur and
Rab, 1997). There may also be a degree of reproductive isolation if cohort life cycles do not overlap. These factors may
promote intraspecific genetic variation within stocks (Anderson
and Rodhouse, 2001). In addition, interspecific genetic differentiation between stocks has not been tested using genetic
markers. Temporal changes, which can also promote both interand intra-genetic differentiation should be tested since temporal divergence has been observed in other ommastrephid squids
(Brierly et al., 1993; Carvalho et al., 1992) like Martialia hyadesi
and Illex argentinus.
The aim of this paper was to evaluate the temporal homogeneity of allele frequencies at one location, and to determine
if there is significant genetic differentiation between populations in order to define the structure of stock populations of
D. gigas.

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E. Sandoval-Castellanos et al. / Fisheries Research 83 (2007) 113118

Table 1
Size, dates and location of the samples used in this study
Code
GY02
MZ01
MZ02
BM03
MCH04
MAN02
HUA02
SP02
CH05
a

#
30
46
32
12
24
10
10
10
36

Locality

Position (long, lat)

S date

Guaymas, Mexico
Mazatlan, Mexico

110 48 W,

Feb/02
Aug/02
Jul/02
Mar/03
May/04
Nov/02
Oct/02
Oct/02
Aug/05

Baha Magdalena, Mexico

Michoacan, Mexico
Mancora, Perua
Huacho Coast, Perua
South of Peruvian Pacfica
Region V, Chile

27 45 N

106 48 W, 23 25 N

106 48 W, 23 25 N
112 06 W, 24 28 N
103 00 W, 17 42 N
8284 0 W, 4 0 S
7981 0 W, 11 30 S
7779 0 W, 16 0 S
7274 0 W, 32 S

Samples kindly donated by C. Yamashiro and R. Tafur from the Instituto del Mar de Peru (IMARPE).

2. Material and methods

A total of 210 samples from mantle or tentacle tissues provided by commercial vessels were analyzed (Table 1 and Fig. 1).
Samples were transported in liquid nitrogen, dry ice, or 70%
alcohol and stored at 70 C in the Laboratorio de Genetica de
Organismos Acuaticos of the Instituto de Ciencias del Mar y
Limnologa in Mexico City.

Genomic DNA was extracted from the tissue samples by

using the Wizard GenomicTM kit (Promega Biosciences Inc.,
San Luis Obispo, CA, USA) and quantified by fluorometry.
PCR reactions and electrophoresis were performed as described
in Daz-Jaimes and Uribe-Alcocer (2003) in a thermalcycler
Mastercycler (Eppendorf AG, Linz GMBH, Hamburg, Germany). Thermocycling parameters were modified to lengthen
annealing and polymerization stages adding 1 s every cycle in

Fig. 1. Sampling location showed in bold with codes used in Table 1. The generalized surface circulation of the eastern Pacific is also showed: California Current
(CAC), North Equatorial Current (NEC), North Equatorial Countercurrent (NECC), South Equatorial Current (SEC), Chile Current (CHC), Peru Current (PC) and
Humboldt Current.

E. Sandoval-Castellanos et al. / Fisheries Research 83 (2007) 113118

order to counteract decreasing activity of the Taq polymerase

associated with longer stages.
Weak, inconsistent and unrepeatable amplification fragments
were not included in the analysis together with fragments with a
null allele frequency lower than 3/S (S = sample size; according to Lynch and Milligan, 1994). Expected heterozygosity
and allele frequencies were calculated by the Taylor expansion
(Lynch and Milligan, 1994).
Due to the limited availability of samples, the temporal analysis was only investigated in two samples taken from one location
(Mazatlan) in two consecutive years (MZ01 and MZ02). Analyses was based on estimation of the population differentiation
statistic (Weir and Cockerham, 1984) and the application of
two statistical homogeneity tests: the exact test of Raymond and
Rousset (1995) and the test proposed by Waples (1989) which
correct error sampling and genetic drift variance. All results
underwent Bonferroni correction (Rice, 1989).
For the geographical structure analysis, eight locations were
compared (see Fig. 1). Genetic variation was estimated by
the genetic diversity of Nei (1973), the effective number of
alleles (Hartl and Clark, 1989), and the information index of
Shannon, which bears a more linear relation with allele frequencies (Shannon and Weaver, 1949), in the POPGENE software (Yeh et al., 1999). In addition, the statistic (Weir and
Cockerham, 1984), and coancestry genetic distances were estimated (Reynolds et al., 1983). A dendrogram with the genetic
distances was built using the UPGMA algorithm. The exact
test was performed for the entire dataset and between sample pairs. Fit to the isolation-by-distance model was tested by
the Mantel test (Sokal and Rohlf, 1995) as implemented in the
TFPGA software (Miller, 1998a). The value, the dendrogram
and the exact test were performed by the program TFPGA.
The genetic structure that splits the populations in two groups:
northern locations (GY02, MZ01/02, BM03 and MCH04) and
southern locations (MAN02, HUA02, SP02 and CH05), was
corroborated by the SAMOVA analysis which tests all possible ways to establish geographic (spatial) groups of populations
to find the sharing that makes a maximum percentage of variation that AMOVA analysis (performed implicitly) attributes
to differentiation between groups (Dupanloup et al., 2002).
This analysis was performed in the SAMOVA software version
1.01 by using the Excoffier distances (Excoffier et al., 1992)
and the dataset made by the program AMOVA-PREP (Miller,
1998b).

115

Table 2
Estimations of genetic diversity by location and for the complete dataset
Code

Ne

GY02
MZ01/02
BM03
MCH04
MAN02
HUA02
SP02
CH05

1.3457 (0.2351)
1.3071 (0.2134)
1.2645 (0.2779)
1.2773 (0.2070)
1.3709 (0.2936)
1.3360 (0.2827)
1.3925 (0.2907)
1.3182 (0.2642)

0.2368 (0.1192)
0.2171 (0.1129)
0.1757 (0.1592)
0.1994 (0.1128)
0.2383 (0.1554)
0.2213 (0.1478)
0.2505 (0.1549)
0.2143 (0.1397)

0.3878 (0.1535)
0.3629 (0.1481)
0.2840 (0.2292)
0.3382 (0.1523)
0.3764 (0.2140)
0.3567 (0.2025)
0.3926 (0.2129)
0.3507 (0.1896)

Total

1.3430 (0.2196)

0.2384 (0.1076)

0.3926 (0.1360)

Standard deviation between parentheses.

3. Results
Seventy-four sharp and reliable bands amplified with five
primers (OPF-1, OPF-3, OPF-4, OPF-5 and OPF-6) were
included in the analysis, out of a total of 124 bands. Their sizes
were between 190 and 1000 bp. The Nei genetic diversity estimator h reached moderate and similar values, between 0.176
(BM03) and 0.251 (SP02), whereas the Shannon index (Table 2)
showed more scattered values between 0.284 (BM03) and 0.393
(SP02). The effective number of alleles in all cases was lower
than two and close to one.
For temporal analysis no significant results were shown by
the Waples test (P = 0.0035) which is equivalent to 0.259 after
correction. The overall probability obtained with the exact test
was P = 0.5477 and the estimated was 0.0129 (bootstrapping
C. I. 0.0022, 0.0259).
In the interpopulation analysis, the overall value of was
0.0809 (C. I. 0.0387, 0.1338). The exact test probability showed
a strong population divergence with an overall value <0.0001.
Values between sample pairs and values showed the same
tendency (Table 3).
In Fig. 2, the UPGMA dendrogram shows two main branches:
northern (GY02, MZ01/02, MCH04 and BM03) and southern
(MAN02, HUA02, SP02 and CH05) (Fig. 3).
The genetic structure found by the SAMOVA that maximized
variation among groups places the northern populations (GY02,
MZ01/02, BM03, and MCH04) in one group and the southern populations (MAN02, HUA02, SP02 and CH05) in another.
This structure attributes 6% of the variation as between-group
variation (Table 4). The fit to the isolation-by-distance model

Table 3
Estimations of (FST ; above the diagonal) and probability obtained with the exact test between sample pairs (under the diagonal)

GY02
MZ01/02
BM03
MCH04
MAN02
HUA02
SP02
CH05

GY02

MZ01/02

BM03

MCH04

MAN02

HUA02

SP02

CH05

0.0008
0.1577
0.2289
0.0132
0.0466
0.0001
<0.0001

0.0194

<0.0001
0.0168
<0.0001
<0.0001
<0.0001
<0.0001

0.0348
0.0768

0.3232
0.6589
0.9953
0.1784
<0.0001

0.0234
0.0146
0.0476

0.0089
0.2732
0.0007
<0.0001

0.1162
0.1506
0.1293
0.1475

1.0000
1.0000
0.8361

0.0650
0.0833
0.0799
0.0767
0.0351

1.0000
0.5866

0.1272
0.1478
0.1450
0.1277
0.0650
0.0540

0.0278

0.1114
0.1165
0.1391
0.1121
0.0367
0.0321
0.0558

Bold letters are used for significant comparisons.

116

E. Sandoval-Castellanos et al. / Fisheries Research 83 (2007) 113118

Fig. 2. UPGMA dendrogram based on genetic distances from coancestry coefficients (Reynolds et al., 1983). The numbers between nodes indicate the percentage of trees sharing the node after 1000 iterations by bootstrapping.

Fig. 3. Isolation of distance tested by means of a Mantel test. Graph that shows
the relation between geographic distances and genetic distances.
Table 4
AMOVA among populations (GY02, MZ01/02, BM03, MCH04, MAN02,
HUA02, SP02 and CH05) and among groups (southern vs. northern)
Types of variance

Among groups
Among populations
Within populations
Among populations
Within populations
Among groups
Within groups

d.f.

Var

Total (%)

SC/ST/CT

1
6
189
7
189
1
195

0.827
0.567
12.065
1.029
12.065
1.032
12.426

6.15
4.22
89.64
7.86
92.14
7.67
92.33

0.045

<0.001

0.104

<0.001

0.061

<0.001

Probability values were obtained from a null distribution of 1000 iterations by

bootstrapping.

was moderate because the comparison between genetic and geographic distances gave a coordination coefficient of r = 0.574
(upper tail probability = 0.992).
4. Discussion
RAPD markers are expected to offer a good representation
of genomic diversity because of their random amplification and
their ability to represent any region of the nuclear genome.

Microsatellite variation is usually greater because of the higher

mutation rate that occurs and previous studies demonstrate that
microsatellite diversity on ommastrephid squids has reached
high values (0.50.95). This conflicts with the low variation (0.010.04) obtained with isozymes (Brierly et al., 1993;
Carvalho et al., 1992). The diversity detected with RAPDs in
this study was moderate (0.23). This is lower than that reported
in Moroteuthis ingens, an oceanic non-ommastrephid squid
(0.31, Sands et al., 2003), but similar to that found in the same
species in the Gulf of California (0.22) by Enriquez-Paredez
(unpublished). Given that D. gigas populations reach several
million individuals (Ehrhardt et al., 1986; Morales-Bojorquez
et al., 1997) it is likely that the real genetic diversity is moderate
to high.
The temporal variation, which was moderate and not significant, could be explained by stochastic processes, genetic drift,
or sampling error.
Some authors point that physical, biological, and oceanographic factors like temperature, high productivity zones, availability of food, and oceanic currents (Brito-Castillo et al., 2000;
Anderson and Rodhouse, 2001) could influence the migrations
and thus the reproductive interchange between populations,
making the dynamics of the genetic differentiation of D. gigas
complex. The first drift of the genetic structure of D. gigas,
given by the UPGMA analysis splits the populations in two
groups: northern and southern. SAMOVA analysis corroborated
that grouping by detecting the sharing proposed as the one that
reach the highest percentage of variation that AMOVA attributes
to differentiation between groups. Although estimations and
homogeneity tests detected differentiation between populations
belonging to the same group, values showed a clear tendency
to be lower between populations of the same group (ranging
from 0.019 to 0.076) and higher between populations of different groups (0.0760.151). Exact test showed a trend of lower P
values between samples belonging to a different group and lower
or non-significant P values between samples of the same group,
with relevant exceptions. The most relevant ones are the comparisons BM03MAN02 (P = 0.66) and BM03HUA02 (P = 0.99).
These could be due to a sampling error because the sample sizes
of the locations were the smaller ones in this study (BM03 = 12;
MAN = 10; HUA = 10). The genetic divergence can be partially
explained by isolation by distance. Although some gene flow
exists it does not occur at a level that prevents genetic differentiation. This may be caused by the adaptation of D. gigas
to different oceanographic regimes (Nigmautllin et al., 2001;
Anderson and Rodhouse, 2001). Trans-hemispheric genetic is
likely to be mediated by oceanographic currents, PeruChile and
California currents direct organisms to the equator, although at
low rates because the currents run towards the western Pacific
moving individuals away from the opposing hemispheres zones
of high productivity/organism density. Inside the groups, the
genetic differentiation is less clear. In the northern group, the
BM03 population appears closer to the GY02 than the MZ01/02,
in disagreement with the geographic distance. In the southern
group, despite its geographic separation, the CH05 population
is not the most genetically isolated population. These patterns
may be partially explained by the currents. In the north, it is

E. Sandoval-Castellanos et al. / Fisheries Research 83 (2007) 113118

possible that a branch of the Californian Current that flows

inside the California Gulf could guide the BM03 population
closer to the GY02 population, while the MZ01/02 population
receives migrants from MICH04 population through action of
the North Equatorial Current. In the south, the lack of a peninsula facilitates gene flow, particularly for the CH05 population,
which may have originated in the southern Peruvian waters and
migrates by the countercurrents of the Peru Current (Anderson
and Rodhouse, 2001).
Isozimes studies in squid of the same subfamily (I. argentinus
and M. hyadesi) have revealed strong geographic and temporal
differentiation, which is considered evidence of a cryptic speciation event (Carvalho et al., 1992; Brierly et al., 1993). However,
the population structuring demonstrated from microsatellite
studies does not suggest such an event is occurring in I. argentinus (Adcock et al., 1999). In this study it was not detected either
a very high or temporal differentiation. However, the detected
structure is high enough to support the suggestion that D. gigas
is in a process of adaptive radiation (Nigmautllin et al., 2001).
The pattern of migration for every cohort in the northern and
southern groups and the genetic differentiations between them
are aspects that have to be studied in further detail. It is necessary that future studies address this question, perhaps through
the use of fine scale markers like microsatellites, in order to
assemble a complete picture about the population structure of
D. gigas.
Acknowledgments
We thank Carmen Yamashiro and Ricardo Tafur from the
Instituto del Mar de Peru (IMARPE) for providing the Peruvian
samples, and to Vicente Anislado for the Michoacan samples.
This project was partially funded by the Program for Projects
of Investigation and Technological Innovation (PAPIIT) of the
National Autonomous University of Mexico (UNAM) (Grant IN
215901). Thanks to Nick Dawnay and Mrinalini Urs for editing
this English-language text.
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