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Spatial and temporal mitochondrial DNA


genetic homogeneity of dolphinfish
populations ( Coryphaena hippurus) in the
eastern central Pacific
ARTICLE in FISHERIES RESEARCH SEPTEMBER 2006
Impact Factor: 1.84 DOI: 10.1016/j.fishres.2006.04.015

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Fisheries Research 80 (2006) 333338

Short communication

Spatial and temporal mitochondrial DNA genetic homogeneity


of dolphinfish populations (Coryphaena hippurus)
in the eastern central Pacific
Pndaro Daz-Jaimes a, , Manuel Uribe-Alcocer a ,
Sofa Ortega-Garca b , Jean-Dominique Durand c
a

Laboratorio de Genetica de Organismos Acuaticos, Instituto de Ciencias del Mar y Limnologa, Universidad Nacional
Autonoma de Mexico, Apdo. Postal 70-305, Mexico D.F. 04510, Mexico
b Departamento de Pesqueras, Centro Interdisciplinario de Ciencias Marinas Instituto Polit
ecnico Nacional,
Apdo. Postal 592, La Paz B.C.S. 23000, Mexico
Institut de Recherche pour le Developpement, UR070-UMR 5171 Station Mediterraneenne de lEnvironnement Littoral 1
quai de la daurade, 34200 S`ete, France
Received 26 January 2006; received in revised form 13 April 2006; accepted 27 April 2006

Abstract
Dolphinfish (Coryphaena hippurus) samples were collected over four consecutive years from four locations in the eastern central Pacific to
evaluate the genetic variation in a 751 bp segment of the mitochondrial NADH subunit 1 (ND1) to test for the presence of genetic population
structure. Sequence analyses revealed no significant differences among collections from the same location in the different years sampled nor
between locations. Mismatch distributions, estimations of population expansion parameters, and neutrality tests revealed significant fluctuations
in population size in coincidence with past glacial and interglacial periods during the late Pleistocene. The low levels of nucleotide diversities
and shallow coalescence of mtDNA genealogies observed were coincident with the estimated demographic parameters and neutrality tests,
in suggesting the presence of important past population size fluctuations or range expansion. The prevention of the accumulation of deep
lineages independently on how it was originated, probably delayed the emergence of a population divergence process which might account
for the lack of genetic differences detected.
2006 Elsevier B.V. All rights reserved.
Keywords: Subpopulations; Historical demography; GENE flow; Population expansion

1. Introduction
The dolphinfish (Coryphaena hippurus) is a cosmopolitan, highly migratory pelagic fish found in tropical and subtropical waters (Palko et al., 1982). The dolphinfish is a
fast growing fish reaching two meters of fork length and
weighting up to 30 kg at 3 years old, and is targeted by both
recreational and commercial fisheries. A significant catch is
taken along the Pacific coast of Mexico by artisanal fisheries,
even though the area within 80 km of the coastline is reserved
Corresponding author. Tel.: +52 55 5622 3899x45382;
fax: +52 55 5616 0748.
E-mail address: pindaro@mar.icmyl.unam.mx (D.-J. Pndaro).

0165-7836/$ see front matter 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.fishres.2006.04.015

by law for sport fishing. However, as there are plans to open


the resource for commercial exploitation, the definition of
the population structure in the fishing area is needed before
proceeding to conduct population dynamics studies to define
management strategies.
Dolphinfish populations are abundant in eastern Pacific
tropical and subtropical areas. Off Mexico, it is distributed
between the Gulf of Tehuantepec and the Baja California
Peninsula, including the Gulf of California.
The seasonality of catch is a feature of dolphinfish populations (Oxenford, 1999; Lasso and Zapata, 1999) and may
be related to seasonal migrations to spawning areas or to seasonal changes in sea temperature. Although no information
about spawning activity is available, spatial and temporal iso-

334

D.-J. Pndaro et al. / Fisheries Research 80 (2006) 333338

lation of spawning groups may result in genetic divergence of


populations. Significant abundance fluctuations in dolphinfish from the Atlantic and Caribbean have been associated
with the presence of divergence between populations, based
on differences in allozyme allele frequencies (Oxenford and
Hunt, 1986). In the Mexican Pacific, large abundances have
been reported around Los Cabos and into the Gulf of California, where important catches are taken from July to
September and from May to August, respectively (Zun igaFlores, 2004). Another area off southern Mexico has also been
recognized in the Gulf of Tehuantepec (off Oaxaca and Chiapas), with maximum abundances during February to May,
(Mendizabal et al., 1990).
Some features of large, pelagic, tropical fish species, such
as their wide distribution, considerable population sizes, high
reproductive potential, dispersal ability, and rapid growth
rates are thought to explain the observed levels of the population structure, which range from shallow, but significant,
structuring to lack of heterogeneity because of the absence
of obvious barriers to dispersal (Graves, 1998; Ward, 2000).
Even though the possible presence of population structure
between populations in a local rather than wide scale could
be remote in the marine realm, clarification of the presence
of discrete genetic populations in the area where the fishery
is taking place is nevertheless important before opening this
fish resource to commercial exploitation.

2. Materials and methods


Samples of dolphinfish tissue were collected at four locations over four consecutive years from small (artisanal)
fishing boats operating in a local scale in the eastern central Pacific (Fig. 1), including Baja California Sur in 2002

(BCS02; N = 16) and 2003 (BCS03; N = 23), Sonora in 2003


(SON03; N = 25), Sinaloa in 2003 (SIN03; N = 21) and 2004
(SIN04; N = 33), and Chiapas in 2003 (CH03; 22), 2004
(CH04; N = 22), and 2005 (CH05; N = 15). Total genomic
DNA was isolated using the proteinase K lysis-buffer
extraction (Laird et al., 1991) and resuspended in 50100 L
of TE buffer.
The complete sequence of the mitochondrial NADH dehydrogenase subunit 1 (ND1) gene of dolphinfish (GenBank
accession number AF272056) was used to design the internal
primers, NADH163 (5 -TAATCCTGCCGCAATTATCC-3 )
and NADH1128 (5 -AGGCCTTCCAGGTTAGGT GT-3 ) to
amplify a 751 pb segment with the polymerase chain reaction
(PCR) in a total of 177 fishes. Reactions for sequencing were
made in total volumes of 100 L containing 10100 ng DNA,
in amplification buffer, 10 mM TrisHCl (pH 8.4), 50 mM
KCl, 1.5 mM MgCl2 , 0.2 mM of each dNTP, 0.1 mM of each
primer and 2.5 U of platinum Taq DNA polymerase (Invitrogen, Cat. 10966-030). PCR amplifications consisted of 35
cycles of 1 min at 95 C for denaturation, 1 min at 58 C for
annealing, and a final extension at 65 C for 3 min. Amplicons were purified with a QIAquick purification kit (QIAgen
No. Cat. 28104) and sequenced on an ABI 3730xl automated
sequencer (Applied Biosystems) by Macrogen Inc., Korea.
Sequences were aligned with ClustalX ver. 1.8 (Thompson et
al., 1997). Identification of an appropriate substitution model
for the mtDNA ND1 gene was made by hierarchical likelihood ratio test implemented in MODELTEST 3.06 (Posada
and Crandall, 1998). Haplotype, h, and nucleotide, , diversities and a minimum spanning network of haplotypes were
estimated with Arlequin (Schneider et al., 1997).
F-statistics (Fst), (Weir and Cockerham, 1984) and ST
(Excoffier et al., 1992), and their respective significance
values were calculated using the Arlequin software with
the Tamura-Nei distances corrected by the gamma-shape
parameter. Arlequin also produced estimates of demographic
parameters , 0 , and 1 from nucleotide mismatch distributions. Fus F, as implemented in Arlequin was used to
test for departures from neutrality due to recent population
expansions or to selection (Fu, 1997). Finally, Harpending
raggedness index (Harpending, 1994) and the sum of squared
deviations (S.S.D.) were used to test for fit to a unimodal
mismatch distribution (Rogers and Harpending, 1992) as
implemented in the Arlequin in order to evaluate the Rogers
sudden expansion model (Rogers, 1995).

3. Results

Fig. 1. Locations of four samples of dolphinfish (Coryphaena hippurus)


from the eastern central Pacific. Sonora (SON), Sinaloa (SIN), Baja California Sur (BCS) and Chiapas (CH).

A 751 base pairs segment of mtDNA ND1 gene was


sequenced for 177 dolphinfishes. A total of 93 variable
sites produced 87 haplotypes. Haplotype diversity averaged h = 0.926, and nucleotide diversity averaged = 0.0052
between samples (Table 1).
The minimum spanning network (MSN) revealed two
clades, each showing a star-like phylogeny centered on two

D.-J. Pndaro et al. / Fisheries Research 80 (2006) 333338

335

Table 1
ND1 mtDNA sequence variability of dolphinfish samples from the eastern central Pacific, and parameters of the sudden population expansion (Rogers and
Harpending, 1992)
Collection

nh

N0

N1

Hri

S.S.D.

SON
SIN
CH
BCS
Total

25
54
59
39
177

18
30
39
24
87

0.94
0.89
0.97
0.92
0.926

0.0034
0.0048
0.0050
0.0053
0.0052

2.664
0.913
1.603
1.861
1.472

147,800
50,600
89,000
103,000
81,600

0.0
2.89
1.979
2.57
2.039

0.0
10.7 103
7.3 103
9.5 103
7.5 103

6655.0
166.0
6512.5
25.4
980.5

2.46 107
6.14 105
2.41 107
9.4 104
3.6 106

0.061
0.012
0.029
0.008
0.016

0.0079
0.0013
0.0069
0.0006
0.0015

Sample size (n), number of haplotypes (nh ), haplotype diversity (h), nucleotide diversity (), Harpendings raggedness index (Hri ) and sum of squared differences
from mismatch analyses (S.D.D.). = 2T, where is the mutation rate of 1.2% for the mtDNA-ND2 region in marine teleosts (Bermingham et al., 1997)
and T is the time since population expansion, 0 = 2N0 before the expansion, 1 = 2N1 after expansion, N is the effective female population size for a initial
population N0, which is assumed to grow to size N1 under the Rogers sudden expansion model and considering a generational time of 3 years for dolphinfish
(Mahon and Oxenford, 1999).

Fig. 2. Minimum spanning network of mtDNA haplotypes in dolphinfish.


Haplotypes are represented with circles showing its frequency per location.
Numbers indicate the number of nucleotide substitutions between haplotypes.

abundant haplotypes (Fig. 2). No apparent temporal or geographic structure appeared between haplotypes.
An AMOVA comparing the four locations showed no variation between temporal samples from the same area over 4
years sampled (ST = 0.02; P = 0.205). No significant spatial
differentiation appeared between locations (SC = 0.011;
P = 0.975) (Table 2). Therefore, collections from each location were pooled to further test for evidence of spatial heterogeneity by pairwise estimates of ST between collections,
Table 2
AMOVA analysis of temporal and spatial genetic variation of mtDNA
sequences for dolphinfish samples from four eastern central Pacific locations
Source of variation

Fixation
indices

Variation (%)

F-statistics

Among groups
Among populations
within groups
Within populations

SC
ST

0.97
1.57

0.009
0.016

0.928
0.261

CT

99.40

0.006

0.107

however no significant differentiation was found for any comparison.


Unimodal mismatch distributions were consistent with
the sudden-population expansion model (raggedness index,
mean = 0.014; range 0.0090.061; S.S.D. = 0.0015, range
0.00060.0079) (Table 1). In addition, values of Fus F (Fu,
1997) were highly significant and negative, indicating deviations from neutrality in all samples (Fig. 3).
Estimates of were similar among locations and in concordance with recent population expansion (Table 2). The
-estimate for the total analyzed sequences was 1.472 (95%
CI 0.4444.771) indicating a population expansion beginning
about 81,000 years ago. The Sinaloa sample showed the most
recent expansion time dated some 50,000 years ago whereas
estimations for the other ranged from 90,000 to 150,000 years
(Table 1). Large differences between 0 and 1 appeared for
the samples Sonora and Chiapas, suggesting rapid population expansions. The value of 0 suggests large initial sizes
for effective female breeders (N0 100,000) for populations
off Baja California Sur and Sinaloa, followed by a moderate
expansion (N1 6.13 105 ) for Sinaloa and a slow expansion
for Baja California Sur (N1 940,000). The populations off
Chiapas showed a large initial effective number of females
(N0 73,000) before expanding rapidly (N1 2.46 107 ),
whereas estimations of the Sonora populations are in concordance with fast expansion (N1 = 2.46 107 ) after a founder
event and-or severe bottleneck (N0 = 0).

4. Discussion
The analyses of a 751 bp segment of the mtDNA ND1
gene in C. hippurus showed spatial and temporal genetic
homogeneity between collections from the reported seasonalabundance areas in the eastern central Pacific. There is a
random distribution of haplotypes between collections suggesting the occurrence of significant gene flow between dolphinfish abundance areas along the eastern central Pacific
coast. Migrations may be facilitated by the predominance of
tropical and subtropical waters in this area during most of
the year, which allows interchange of dolphinfish individuals
between different areas.

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D.-J. Pndaro et al. / Fisheries Research 80 (2006) 333338

Fig. 3. Fus F and its probability (Fu, 1997), pairwise mismatch distributions, and its fit to the Rogers model of sudden expansion (simulated) for each location.

However, genetic differentiation in marine fish may also


be affected by the historical demography of populations
(Lecomte et al., 2004; Ely et al., 2005). Recent colonization processes have a strong effect on both genetic diversity
and mtDNA gene genealogy lineages. Pleistocene glacial
cycles produced recurring shifts in sea surface temperatures
off Mexico (Lea et al., 2000) and may have influenced dolphinfish populations.
Nucleotide diversities between samples were low, while
haplotype diversities were high, resulting from two abundant
haplotypes and a star-like phylogeny. Low nucleotide diversities reflect the predominance of a single or few haplotypes and
numerous low-frequency haplotypes separated by only a few
mutations. This pattern can be associated with previous habitat reductions or with population bottlenecks. Low mtDNA
nucleotide diversities and shallow genealogies also appear in
many pelagic fishes, including billfish and other cosmopolitan fishes, and may be associated with glacial episodes (Grant
and Bowen, 1998 and references therein).
The fit to the sudden expansion model in eastern Pacific
dolphinfish collections may also reflect recent colonizations
from warm refugia and population expansions following
Pleistocene coolings.
During the late Pleistocene, over the past 200,000 years,
two main glaciations occurred (Wisconsin and Illinois),
decreasing sea surface temperature by 2.8 C in the eastern tropical Pacific (Lea et al., 2000). These periods of
cooling were followed by interglacial episodes characterized by warm sea surface waters in the Pacific (Stott et al.,
2002), especially the eastern Pacific where extreme ENSO-

like episodes occurred (Lea et al., 2002). During those


oscillations, dolphinfish likely experienced several cycles of
contractionexpansion. Since such episodes have been recurrent during last hundreds of thousands of years, times since
expansions began have not been long enough to allow the
populations to become differentiated.
Samples of dolphinfish analyzed in the eastern Pacific have
similar times since population expansion and similar numbers
of colonizers, or bottleneck survivors, with the exception of
the near Sonora populations, which was the result of a founder
event ( 0 = 0) followed by a rapid expansion. The expansion
in populations near the southernmost sample, Chiapas located
in tropical waters, experienced a more recent and rapid expansion, although some multimodal pattern was observed from
pairwise mismatch distribution suggesting an older origin and
size stability which maybe related with its tropical localization.
The expansions in areas adjacent to the mouth of the Gulf
of California (BCS and Sinaloa) have been small and slow
as shown by the small differences between 0 and 1 and
from estimations of the initial number of females. This pattern may be the result of the heterogeneity in oceanographic
conditions prevalent in that area, where the mix of cold water
masses from the California Current and warmer waters from
the Gulf of California occurs. There is a seasonal predominance of tropical waters during summer in the southern part
of the Gulf of California, whereas conditions into the Gulf of
California that are influenced by the influx of tropical waters
are more stable during the year, with favorable conditions for
dolphinfish similar to those present in tropical areas.

D.-J. Pndaro et al. / Fisheries Research 80 (2006) 333338

Unimodal pairwise mismatch distributions and starshaped gene genealogies may also result from recent range
expansion events followed by high gene flow between populations (Excoffier, 2004) or heterogeneity in mutation rate
in highly variable regions (Schneider and Excoffier, 1999).
Presence of warm water associated with the occurrence of
El Nino events during at least thousands of years, have
offered opportunities for colonization of new areas and hence
range expansions. Shifts in the distributions of dolphinfish
related to periods of high sea surface temperatures have
been inferred from increased catches during periods of high
sea temperatures in summer during El Nino years off
southern California (Norton, 1999). The Chiapas sample
displayed a slight pattern of multimodal pairwise mismatch
distribution in agreement with a range expansion. Likewise
the large population size estimated for this sample and hence
of a larger number of potential migrants, provides further
evidence of range expansion (Excoffier, 2004). Therefore,
because their tropical localization, populations off Chiapas
might have represented the center of dispersion for northern
dolphinfish distributed in temperate waters until sea surface
temperature increased during interglacial periods. Nevertheless, in the absence of a wider picture of the diversity
distribution in C. hippurus it is not possible to discard
between the bottleneck assumption and the range expansion
one.
Results presented here, show evidence about the demographic history of eastern Pacific dolphinfish and/or range
expansions which has evidently influenced patterns of
genetic variability of mtDNA and could reduce the chance to
recovering a signal of genetic isolation between seasonally
separated abundance areas. Hence, surveys of nuclear
markers which have larger effective population sizes may
provide greater amount of resolution to for detect the
signal of divergence in case those differences in seasonal
abundance correspond to structured populations. Consequently, the population expansion signal observed beside
the genetic homogeneity documented in the present study,
should not be interpreted as evidence of high population size
for dolphinfish. A precautionary approach is needed until
further data confirms the panmictic condition of dolphinfish
population before considering their commercial exploitation.

Acknowledgements
This study was funded by the Programa de Apoyo
a Proyectos de Investigacion e Innovacion Tecnologica,
DGAPA-UNAM, grant IN227403. We are grateful to
Erika Mojica Quezada, Evangelina Castillo Olgun, Monica
Domnguez Lopez, and Francisco Sancho for collecting and
processing samples. Thanks to the two anonymous reviewers who provided valuable comments and improved notably
the manuscript and to Ellis Glazier for editing the Englishlanguage text.

337

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