Molecular Insights Into the Population Structures of Cosmopolitan Marine Fishes
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Molecular Insights Into the Population
Structures of Cosmopolitan Marine Fishes
J. E. Graves
Many marine fishes are cosmopolitan, occurring in continuous (e.g., circumtropi-
cal) or discontinuous (e.g., antitropical) distributions. Little is known of the genetic
basis of population structure of these species, even though several support exten-
sive fisheries. To develop a database that would facilitate comparison of the pop-
ulation structures among cosmopolitan fishes we consistently included restriction
fragment length polymorphism (RFLP) analysis of mitochondrial DNA (mtDNA) as
a common approach to our investigations of these species. This article presents a
review of those analyses. Considerable intraspecific genetic variation was revealed
within all cosmopolitan marine species. Continuously distributed species displayed
population structures ranging from a lack of significant heterogeneity between
ocean samples to shallow but significant structuring within an ocean basin. In gen-
eral, greater intraspecific genetic divergence was revealed within discontinuously
distributed fishes. Levels of population structuring ranged from species compris-
ing conspecific populations with no mtDNA haplotypes in common to those com-
prising populations with homogeneous distributions of mtDNA haplotypes across
ocean basins. The close affinity of haplotypes among conspecific populations of
all discontinuously distributed species was consistent with contact since the Pleis-
tocene. Although general patterns of genetic population structure were similar
among continuously and discontinuously distributed cosmopolitan marine species,
there were some striking differences. These differences underscore the need for a
thorough understanding of the genetic basis of population structure of each spe-
cies for proper management.
Several species of pelagic marine fishes albacore (Graves and Dizon 1989) than
are broadly distributed, inhabiting the was reported between populations of ter-
tropical and subtropical surface waters of restrial organisms separated by as little as
the world’s oceans ( Briggs 1960). Some of tens or hundreds of kilometers (e.g., Avise
these species, including tunas, billfishes, et al. 1979). Although the small sample
swordfish, dolphin fish, and several sharks, sizes employed in those studies limited
support extensive commercial and recre- the power of the analyses to critically test
ational fisheries throughout their ranges. the null hypothesis that Atlantic and Pa-
Little is known of the population genetic cific populations shared a common gene
structure of any of these truly internation- pool, we were impressed by the absence
al fishery resources, although such infor- of consistent genetic differences between
From the Virginia Institute of Marine Science, P.O. Box
1346, Gloucester Point, VA 23062. I am indebted to my mation is critical to the delineation of fish- samples of skipjack tuna and albacore
colleagues Jan McDowell, Dan Scoles, Jan Cordes, Cath- ery management units, the evaluation of from different oceans, and suggested that
erine Goodbred, and Bruce Collette who coauthored fishery interactions, and on a longer time the relative lack of genetic divergence
the manuscripts upon which this review is based. I
gratefully acknowledge the many individuals who as- scale, the conservation of genetic varia- might be attributed to either recent isola-
sisted in sample collection. This manuscript benefited tion (Allendorf et al. 1987; Avise 1996). tion or a low level of contemporary gene
from the critical reading of Vince Buonaccorsi, David
Carlini, Kimberly Reece, and two anonymous review-
Over the past several years our labora- flow. The latter would be facilitated by the
ers. Funds for this study were provided by the National tory has investigated the stock structure presence of a continuous circumtropical
Marine Fisheries Service and the Billfish Foundation. of many continuously distributed pelagic habitat, the occurrence of spawning over
VIMS contribution no. 2133. Address correspondence
to Dr. Graves at the address above or e-mail: fishes. Preliminary studies employing re- a broad spatial and temporal range, and
graves@vims.edu. This paper was delivered at a sym- striction fragment length polymorphism the species’ potential for intraspecific
posium entitled ‘‘Conservation and Genetics of Marine (RFLP) analysis of mitochondrial DNA gene flow mediated by passive larval dis-
Organisms’’ sponsored by the American Genetics As-
sociation at the University of Victoria, Victoria, BC, (mtDNA) revealed less genetic divergence persal or the high vagility of adults.
Canada, June 7, 1997. between Atlantic and Pacific populations In the 1980s there were few mtDNA-
1998 The American Genetic Association 89:427–437 of skipjack tuna (Graves et al. 1984) and based population genetic analyses of ma-
427rine fishes with which to compare our re-
sults. Because of the large potential for
gene flow in the pelagic environment, we
felt that there was limited value to com-
parisons of the population structures of
highly vagile cosmopolitan marine fishes
with those of freshwater fishes or terres-
trial animals which often have greatly re-
duced dispersal abilities and encounter
formidable barriers to gene flow within
their ranges. Therefore, to develop a more
appropriate database with which to com-
pare our continuing studies of circumtrop-
ical pelagic fishes, we initiated investiga-
tions of the population genetic structure
of broadly distributed pelagic marine fish-
es with disjunct populations. Several spe-
cies of temperate marine fishes are known
to comprise geographically isolated con-
specific populations north and south of
the tropics ( Briggs 1974). We assumed
that, relative to continuously distributed
pelagic fishes, those with antitropical dis-
tributions would display more population
genetic structure, but not nearly as much
as that reported among most conspecific
populations of freshwater fishes or terres-
trial animals. In addition, the ability to es-
timate a time of divergence for isolated
conspecific populations of temperate fish-
es using analyses of allozymes (Grant and
Leslie 1996; Stepien and Rosenblatt 1996)
or mtDNA ( Bowen and Grant 1997) would
provide temporal reference points to eval-
uate genetic divergences among popula-
tions of continuously distributed pelagic
fishes.
Cosmopolitan Marine Fishes
This review focuses on studies of four
‘‘species’’ with circumtropical distribu-
tions: yellowfin tuna (Scoles and Graves
1993), white/striped marlin (Graves and
McDowell 1994, unpublished data), blue
marlin (Graves and McDowell 1995, un-
published data) and sailfish (Graves and
McDowell 1995; McDowell JR and Graves
JE, unpublished data); and four species of
cosmopolitan temperate fishes with dis-
junct distributions: bluefish (Goodbred
and Graves 1996) and three species of
mackerels (Scoles et al., in press).
Yellowfin Tuna Figure 1. Distribution of cosmopolitan marine fishes. (a) Circumtropical distributions. The shaded area reflects
the distribution of yellowfin tuna (T. albacares), blue marlin (M. nigricans), sailfish (I. platypterus), striped marlin
Yellowfin tuna (Thunnus albacares) occur (T. audax, Indo-Pacific Oceans), and white marlin (T. albidus, Atlantic Ocean). The distributions of yellowfin tuna,
throughout the tropical and subtropical striped marlin, and white marlin extend a little further into subtropical waters than those of blue marlin or sailfish.
(b) Bluefish (P. saltatrix). (c) Atlantic mackerel (S. scombrus, stippled shading) and spotted chub mackerel (S.
waters of the Atlantic, Indian, and Pacific australasicus, lined shading). (d) Chub mackerel (S. japonicus).
Oceans ( Figure 1a), rarely entering areas
with surface water temperatures below
18⬚C (Collette and Nauen 1983). Spawning
occurs throughout the year over a broad
428 The Journal of Heredity 1998:89(5)area in the tropical oceans. Individuals ex- (Prince et al. 1991). It is estimated that in- cific ( Figure 1b). Bluefish attain a maxi-
hibit relatively rapid growth, attaining a dividuals may live in excess of 20 years. A mum size in excess of 10 kg, and individ-
length of 100 cm at the end of 2 years. Yel- strong sexual dimorphism is evident in the uals typically reach sexual maturity during
lowfin tuna are typically mature by the species, with males typically reaching their second year (Wilk 1977). Depending
end of their second year and may live for maximum sizes of less than 120 kg, while on the population, spawning may occur in-
at least 8 years ( Inter-American Tropical females may exceed 800 kg ( Nakamura shore or in waters extending to the edge
Tuna Commission 1991). Yellowfin tuna 1985). Tagging studies reveal that most of the continental shelf. Larvae exist in the
are vagile, and tagging studies indicate fish are recaptured near their site of re- plankton for up to 30 days and in some
that some individuals undertake extensive lease, despite several years of freedom areas rely on cross-shelf transport to ar-
movements, including trans-Atlantic mi- (Witzell and Scott 1990). Some individuals rive in estuarine nursery areas ( Hare and
grations (Scott et al. 1990), although the have been known to undertake extensive Cowen 1993). Seasonal migrations are
majority of fish are recovered within sev- movements within ocean basins, and in common within each population, and
eral hundred kilometers from the point of two instances, between oceans ( NMFS tagged individuals have been reported to
release ( Hunter et al. 1986). 1994). Little is know of spawning in the travel in excess of 1300 km ( Lund and Mal-
blue marlin. Mature individuals and larvae tezos 1970). It is not known if migration
Istiophorid Billfish have been captured over a broad range in occurs among geographically distinct pop-
The family Istiophoridae comprises three the tropics (Matsumoto and Kazama 1974; ulations.
genera: Makaira ( blue marlin and black Strasburg 1969). However, evidence for
marlin), Tetrapturus (white marlin, striped distinct spawning cycles has been report- Mackerel
marlin, and at least three species of spear- ed in some areas near island chains ( Hop- Three species of mackerels are recognized
fish), and Istiphorus (sailfish). All are epi- per 1990). in the genus Scomber. The Atlantic mack-
pelagic predators with extensive ranges in The sailfish (Istiophorus platypterus), like erel (S. scombrus) is found in the North At-
tropical and subtropical marine waters. the blue marlin, exhibits a circumtropical lantic ( Figure 1c), spotted chub mackerel
The striped marlin (Tetrapturus audax) distribution ( Figure 1a) and has been rec- (S. australasicus) is found in the Indian and
and the white marlin (T. albidus) have ognized by some authors as comprising Pacific Oceans ( Figure 1c), and the chub
ranges that extend a little further into sub- Atlantic and Indo-Pacific species ( Naka- mackerel (S. japonicus) is found in the
tropical waters than the other istiophorids mura 1985). Genetic data are consistent temperate waters of all three oceans ( Fig-
( Figure 1a; Nakamura 1985). The white with the existence of a single species ure 1d). Each species comprises multiple,
marlin is restricted to the Atlantic Ocean (Graves and McDowell 1995). Sailfish tend disjunct populations. Comprehensive bio-
and reaches a maximum size of approxi- to be distributed more coastally than blue logical information is not available for all
mately 80 kg, while the striped marlin oc- marlin, although they are taken on long- three species, or for the different geo-
curs in the Indian and Pacific Oceans and line gear in commercial fisheries through- graphical populations of each species. In
reaches a maximum size of approximately out the tropical oceans. The maximum general, mackerels are coastal, schooling
200 kg. Little is known of the spawning size reached by individuals varies among fishes that feed on plankton and small fish-
habits of either species, although ripe in- locations within and between oceans. es. Maximum size for each species is ap-
dividuals and early life-history stages have Maximum sizes of approximately 60 kg proximately 50 cm fork length (generally
been found over a broad region in tropical and 100 kg have been reported for the At- less than 2 kg), and sexual maturity is
waters. Tagging studies indicate that indi- lantic and Pacific Oceans, respectively reached in 2–3 years (Collette and Nauen
viduals of both species are capable of ex- ( Nakamura 1985). The recapture of a 1983). All three species are serial spawn-
tended movements, including trans-Atlan- tagged fish 16 years after release indicates ers and the duration of the larval stage is
tic migrations of white marlin and recov- that individuals can be long-lived. Tagging 3–4 weeks ( Hunter and Kimbrell 1980;
eries in Hawaii of striped marlin tagged off studies also demonstrate the potential for Ware and Lambert 1985).
California (Scott et al. 1990; Squire 1987). extended movements (in excess of 2000
As with the other isotiophorids, a large km), although the majority of recaptures
Genetic Analyses
fraction of white and striped marlin are re- are in the same area as the release (Scott
captured near the site of release even after et al. 1990). Sailfish are multiple spawners, A wide variety of molecular genetic tech-
several years. Trends in tag-recapture data and spawning has been reported in off- niques are currently available to popula-
reveal seasonal movements within areas, shore waters as well as a number of loca- tion geneticists (Avise 1994), and several
some of which may be related to spawning tions throughout the species’ range. In have been used to survey variation of nu-
in tropical waters (Squire and Suzuki some areas spawning activity occurs clear and mitochondrial loci within pelag-
1990). throughout the year, while in other ic fishes. The large number of techniques
The blue marlin (Makaira nigricans) is regions it is restricted to a period of sev- and loci available for genetic analyses en-
an epipelagic predator occurring through- eral months ( Nakamura 1985). ables the selection of genetic loci and an-
out tropical oceans ( Figure 1a). Various alytical methods that are best suited to re-
authors have separated blue marlin into Bluefish veal population structure within the par-
an Atlantic and an Indo-Pacific species The bluefish (Pomatomus saltatrix) is a pe- ticular species of interest. Unfortunately
( Nakamura 1985); however, recent genetic lagic predator commonly found in temper- this same diversity reduces the opportu-
data support the existence of a single spe- ate coastal marine waters at temperatures nity for comparative studies of population
cies ( Finnerty and Block 1992; Graves and between 15⬚C and 25⬚C (Wilk 1977). The structure across taxa as, more often than
McDowell 1995). Blue marlin exhibit very species comprises at least six geographi- not, different studies have surveyed differ-
rapid growth and reach a total length of cally distinct populations and is found in ent loci with different techniques. Realiz-
almost 2 m by the end of their first year most ocean basins except the eastern Pa- ing the need for comparative studies with-
Graves • Population Structures of Cosmopolitan Marine Fishes 429in the discipline, we have consistently em- Table 1. Sample sizes, the number of geographically distant collection locations in the Atlantic (A),
Pacific (P), and Indian (I) Oceans, and genetic variation of cosmopolitan marine fishes
ployed RFLP analysis of the entire mtDNA
genome as one approach in our investi- Collection Haplotype diversity, Mean nucleotide sequence
gations of genetic variation within cos- Species locations N h (sample range) diversity, (sample range)
mopolitan marine fishes. Yellowfin tuna 1A, 5P 120 0.84 (0.82–0.87) 0.28% (0.28–0.39%)
Striped marlin 4P 166 0.82 (0.69–0.84) 0.30% (0.20–0.32%)
Methodology White marlin 4A 235 0.78 (0.54–0.90) 0.15% (0.06–0.15%)
Blue marlin 3A, 3P 424 0.91 (0.58–0.97) 0.59% (0.14–0.80%)
Detailed descriptions of sample collec- Sailfish 2A, 1P, 1I 109 0.59 (0.28–0.73) 0.40% (0.22–0.66%)
tions and analytical protocols for each Bluefish 4A, 1P, 1I 150 0.92 (0.10–0.92) 1.09% (0.05–0.71%)
Atlantic mackerel 2A 40 0.58 (0.28–0.85) 0.18% (0.07–0.29%)
species are provided in the primary pub- Spotted chub mackerel 4P, 1I 93 0.86 (0.59–0.86) 1.90% (0.13–0.77%)
lications. For most specimens mtDNA was Chub mackerel 4A, 4P 276 0.96 (0.64–0.95) 2.48% (0.29–0.50%)
purified from heart and gonad tissue dis-
sected from individuals within 8 h of cap-
ture using the equilibrium density gradi-
ent centrifugation protocols of Lansman et mogeneity using the chi-square random- lated to all other geographically isolated
al. (1981). In cases where yields of purified ization method of Roff and Bentzen (1989). populations of bluefish. Pairwise compar-
mtDNA were low, mtDNA-enriched geno- All of the above calculations were per- isons of the Brazilian bluefish with the five
mic DNA was isolated using the protocols formed with the restriction enzyme anal- other populations resulted in net mean nu-
of Chapman and Powers (1984). The ysis package (REAP) of McElroy et al. cleotide sequence divergences greater
mtDNA samples for each species were in- (1992). than ␦ ⫽ 1.38%.
dividually digested with a suite of 9 to 12
restriction endonucleases and the result- Atlantic Mackerel
Population Genetic Structuring
ing fragments were separated electropho- Collections of 20 Atlantic mackerel each
Within Cosmopolitan Species With
retically overnight on agarose gels. Frag- were obtained from the western North At-
Discontinuous Distributions lantic ( U.S.) and eastern North Atlantic
ments of purified mtDNA were end-labeled
with 35S radionucleotides prior to electro- Bluefish ( England). Within-sample variation re-
phoresis and subsequently visualized by Samples of bluefish were obtained from vealed by RFLP analysis of mtDNA using
autoradiography (Sambrook et al. 1989). six geographically isolated populations; 12 restriction enzymes was greater in the
Gels containing digestions of mtDNA-en- four within the Atlantic Ocean ( U.S., Por- western Atlantic (h ⫽ 0.85) than the east-
riched genomic DNA isolations were trans- tugal, Brazil, and South Africa), one from ern Atlantic (h ⫽ 0.28) ( Table 1). A single
ferred to a solid support (Southern trans- the Pacific Ocean (eastern Australia), and haplotype was common to both samples,
fer) and hybridized with a biotin-labeled one from the Indian Ocean (western Aus- occurring in a majority of individuals from
probe DNA consisting of mtDNA purified tralia). RFLP analysis of mtDNA employing the eastern North Atlantic (0.85) and at a
from conspecifics or the entire yellowfin nine informative restriction endonucleas- lower frequency in the U.S. collection
tuna mtDNA molecule cloned as four frag- es revealed a broad range of within-sam- (0.35), but the distribution of haplotypes
ments into a plasmid vector. ple diversities among locations ( Table 1). was not homogeneous between the sam-
Each different fragment pattern pro- Five of the six bluefish collections exhib- ples. The rare haplotypes in both collec-
duced by a restriction endonuclease was ited relatively high levels of variation, with tions were closely related to the common
assigned a letter, and relationships among haplotype diversities in excess of h ⫽ 0.66. haplotype (differing by the gain or loss of
patterns were inferred from completely However, the two collections of 19 fish one or two restriction sites), resulting in a
additive fragment sizes. A composite each obtained from eastern Australia in net nucleotide sequence divergence of ␦ ⫽
mtDNA haplotype consisting of 9 to 12 let- 1991 and 1995 displayed greatly reduced 0.01% ( Figure 2).
ters representing the fragment patterns genetic variation. Both collections com-
generated by each restriction endonucle- prised two haplotypes, one of which was Spotted Chub Mackerel
ase was compiled for every individual. represented by 18 individuals in each sam- Five collections of 15 to 21 spotted chub
Haplotype diversity (h), which represents ple, resulting in similar haplotype diversi- mackerel were obtained from the western
the probability of encountering different ties of h ⫽ 0.10. North Pacific (Japan), eastern North Pacif-
haplotypes in multiple draws from a sam- No haplotypes were shared among any ic (Mexico), western South Pacific (Aus-
ple, was calculated following Nei (1987). of the six isolated collections of bluefish, tralia and New Zealand), and Red Sea ( Is-
Nucleotide sequence divergence (d) be- although geographically proximate collec- rael). Haplotype diversities (h) were fairly
tween mtDNA haplotypes was estimated tions often contained haplotypes that dif- similar among the samples, varying be-
from a restriction site presence/absence fered by the gain or loss of a single restric- tween 0.59 and 0.85 ( Table 1), but the
matrix using the approach of Nei and Mil- tion site. Bluefish from the western and mean nucleotide sequence diversities of
ler (1990). Mean nucleotide sequence di- eastern North Atlantic ( U.S. and Portugal) the Australia and New Zealand collections
versity within samples (), which is the were closely related (␦ ⫽ 0.26%), as were ( ⫽ 0.75% and 0.77%, respectively) were
weighted sequence divergence among those from eastern and western Australia elevated relative to those from Japan,
haplotypes within a sample, and the mean (␦ ⫽ 0.42%) ( Figure 2). The South African Mexico, and the Red Sea ( ⫽ 0.30%,
nucleotide sequence divergence between collection was most closely associated 0.13%, and 0.41%, respectively). This dif-
samples corrected for within-sample di- with those from the western and eastern ference resulted from the presence of two
versity (␦) were calculated following Nei North Atlantic (␦ ⫽ 0.38% and 0.35%, re- divergent mtDNA lineages within the Aus-
(1987). The distribution of haplotypes spectively). Bluefish from the western tralia and New Zealand samples. The hap-
among collections was evaluated for ho- South Atlantic ( Brazil) were distantly re- lotypes from the different lineages differed
430 The Journal of Heredity 1998:89(5)by an average nucleotide sequence diver- between the two samples. In the eastern At- distribution of haplotypes was not. Several
gence of d ⫽ 1.34%. One of the lineages lantic the distribution of haplotypes among haplotypes occurred at elevated frequencies
was unique to the samples from Australia collections from the Mediterranean Sea, Ivo- either in single collections or in combined
and New Zealand. Three haplotypes were ry Coast, and South Africa was not signifi- collections from the eastern Pacific or west-
common to those samples and the distri- cantly heterogeneous. Similarly, heteroge- ern/central Pacific (Table 2). Values of net
bution of haplotypes between the two lo- neity was not observed between samples nucleotide sequence divergence (␦) be-
cations was not significantly heteroge- from Argentina and the Ivory Coast, across tween samples were very low, ranging from
neous. the South Atlantic. 0.01% to 0.06% (Figure 3). This resulted from
Collections of spotted chub mackerel Net nucleotide sequence divergences the relatively high levels of within- sample
from Japan and Mexico in the North Pacif- greater than ␦ ⫽ 1.17 % separated all At- variation and the close affinity of most hap-
ic shared two haplotypes, one of which oc- lantic and Pacific samples of chub mack- lotypes, which typically differed by the gain
curred at elevated frequencies in both erel ( Figure 2). Within the western North or loss of one or two restriction sites.
samples. Although the two samples were Pacific the distribution of haplotypes was
separated by a small net nucleotide diver- not significantly heterogeneous between White Marlin
gence of ␦ ⫽ 0.02%, the distribution of collections from Taiwan and Japan. Four Four relatively large collections of white
haplotypes was not homogeneous be- haplotypes were common to these collec- marlin were obtained from geographically
tween the samples (P ⫽ .013). tions, three of which occurred in more distant locations within the Atlantic Ocean
One haplotype was common to all four than one individual in each sample. The ( U.S., Caribbean, Brazil, and Morocco).
Pacific samples of spotted chub mackerel, combined western North Pacific samples RFLP analysis of mtDNA employing 12 re-
occurring at low frequencies in the South exhibited one fixed restriction site differ- striction endonucleases revealed substan-
Pacific and elevated frequencies in the ence relative to the sample from Califor- tial within-sample variation (h ⫽ 0.54–
North Pacific. A net nucleotide sequence nia, and were separated by a net nucleo- 0.90) but reduced nucleotide sequence di-
divergence of ␦ ⫽ 0.54% separated the tide sequence divergence of ␦ ⫽ 0.30%. versities ( ⫽ 0.15–0.30%) due to the very
combined North Pacific and South Pacific close relationships of the haplotypes. No
samples ( Figure 2), reflecting the presence spatial partitioning of genetic variation
Population Genetic Structuring
of the divergent mtDNA lineage in the was evident among the four collection lo-
Within Cosmopolitan Species With
South Pacific samples. cations. Seven haplotypes were represent-
Continuous Distributions
The Red Sea collection of spotted chub ed by four or more individuals in the
mackerel possessed haplotypes that were Yellowfin Tuna pooled sample of 235 white marlin, and six
intermediate to those of Pacific spotted Five collections of 20 yellowfin tuna each of these were common to all four geo-
chub mackerel and Atlantic chub macker- from the Pacific (Mexico, Ecuador, Hawaii, graphically distant samples. No major dis-
el. The Red Sea sample was most closely Papua New Guinea, and Australia) and one continuities in haplotype frequencies were
related to the South Pacific samples of from the Atlantic ( U.S.) were analyzed noted between samples across the Atlan-
spotted chub mackerel (␦ ⫽ 0.51%), in par- with 12 restriction enzymes. Variation was tic or across the equator, and net genetic
ticular, the mtDNA lineage that was unique strongly conserved across all samples. divergences (␦) between samples were all
to the Australia and New Zealand samples. Haplotype diversities (h) ranged from 0.82 less than 0.01%.
The Red Sea mackerel collection was orig- to 0.87, and mean nucleotide sequence di-
inally described as chub mackerel (S. ja- versities () varied from 0.28% to 0.39%. White/Striped Marlin
ponicus) based on morphology and the re- Several haplotypes were shared among all Ten restriction endonucleases were com-
ported distribution of the species of Scom- collections of yellowfin tuna, including mon to the RFLP analyses of white and
ber (Matsui 1967). However, both RFLP those from different oceans ( Table 2). The striped marlin, allowing an evaluation of
analysis of mtDNA and sequencing of the two most common haplotypes were rep- interocean genetic divergence between
mitochondrial cytochrome-b gene re- resented by approximately one-half of the the two species. Surprisingly, two haplo-
vealed that the Red Sea mackerels were individuals in each sample. The distribu- types were common to both species, one
more closely aligned with spotted chub tion of haplotypes among the five samples of which occurred in white marlin at a fre-
mackerel. A subsequent morphological ex- of yellowfin tuna within the Pacific Ocean quency of 0.73 and in striped marlin at a
amination of mackerel from the Red Sea and the single Atlantic sample was not sig- frequency of 0.13. Furthermore, the most
and northern Indian Ocean has resulted in nificantly heterogeneous, and the net nu- common white marlin haplotype differed
a reassignment to S. australasicus ( Baker cleotide sequence divergences (␦) be- by a single site change from the most com-
and Collette, 1998). tween samples were quite small, ranging mon striped marlin genotype. Neighbor-
from 0.01% to 0.10% ( Figure 3). joining and parsimony analyses revealed
Chub Mackerel no clustering of haplotypes by ocean (spe-
Eight collections of chub mackerel were an- Striped Marlin cies), and the white marlin and striped
alyzed, five from the Atlantic Ocean and Four Pacific collections of approximately 40 marlin were separated by a net nucleotide
three from the Pacific Ocean. Several hap- striped marlin from Mexico, Ecuador, Ha- sequence divergence of 0.12% ( Figure 3).
lotypes were common to two or more sam- waii, and Australia, each exhibited about the
ples within the Atlantic. Along the western same level of within-sample variation. Hap- Blue Marlin
Atlantic, samples from the United States and lotype diversities (h) varied between 0.69 Blue marlin collections from the Atlantic
Argentina shared one haplotype and were and 0.84, and mean nucleotide sequence Ocean ( U.S., Jamaica, and Brazil) and Pa-
separated by a small net nucleotide diver- mean diversities () ranged between 0.20% cific Ocean (Mexico, Ecuador, Hawaii, and
gence (␦ ⫽ 0.04%), but the distribution of and 0.32% (Table 1). Although the level of Australia) exhibited high levels of within-
haplotypes was significantly heterogeneous variation was similar among samples, the sample variation ( Table 1). Atlantic sam-
Graves • Population Structures of Cosmopolitan Marine Fishes 431Table 2. Distribution of mtDNA haplotypes
among collections of yellowfin tuna (YFT) and
striped marlin (STM)
Genotype MEX ECU HAW AUS PNG ATL
YFT-1 6 7 7 8 8 7
YFT-2 5 2 3 4 3 3
YFT-3 — 3 1 — 1 1
YFT-4 1 1 — 2 — 2
YFT-5 — — — 1 1 2
YFT-6 — 1 1 — — 1
YFT-7 1 2 — — — —
YFT-8 2 — — 1 — —
Minor 5 4 8 4 7 4
Total 20 20 20 20 20 20
STM-1 12 20 14 12
STM-2 6 6 7 3
STM-3 8 9 4 1
STM-4 — 2 10 8
STM-5 — 1 2 7
STM-6 — 1 — 11
STM-7 6 — — —
STM-8 — — 3 —
Minor 4 1 3 5
Total 36 40 43 47
Minor haplotypes occurred in two or fewer individuals
in the pooled sample.
ples of blue marlin consistently exhibited
higher mean nucleotide sequence diversi-
ties than Pacific collections (pooled Atlan-
tic ⫽ 0.74%, pooled Pacific ⫽ 0.18%).
This was due to the presence of two ge-
netically distinct mtDNA lineages within
the Atlantic samples, only one of which
was represented in Pacific collections. The
unique Atlantic haplotypes typically dif-
fered from the ‘‘ubiquitous’’ haplotypes by
five or more restriction site differences,
and an average nucleotide sequence di-
vergence of 1.23%.
No significant geographic population
structuring was revealed among blue mar-
lin samples within the Atlantic or Pacific
Oceans. Almost all haplotypes represent-
ed by more than a few individuals were
common to two or more collections, and
no significant heterogeneity was observed
in the distribution of haplotypes among
collections within an ocean.
Significant heterogeneity was evident,
however, in the distribution of haplotypes
between collections of blue marlin from Figure 2. UPGMA clustering of net mean nucleotide sequence divergences (␦) among populations of four species
the Atlantic and Pacific Oceans. This was of discontinuously distributed pelagic marine fishes: bluefish (P. saltatrix), Atlantic mackerel (S. scombrus), spotted
chub mackerel (S. australasicus), and chub mackerel (S. japonicus).
due primarily to the presence of the
unique lineage of haplotypes within the
Atlantic which occurred in approximately the Pacific sample exhibiting values con- cleotide sequence divergence of 0.27%
40% of the Atlantic blue marlin. A net nu- siderably lower than the other collections. separated Atlantic and Indo-Pacific collec-
cleotide sequence divergence of 0.15% Two genetically distinct clades of haplo- tions ( Figure 3).
separated the Atlantic and Pacific collec- types were present within Atlantic sam-
tions ( Figure 3). ples, with only one occurring in samples
Phylogeographic Patterns Among
from the Pacific or Indian Oceans. The At-
Cosmopolitan Species
Sailfish lantic clade haplotypes occurred in ap-
Sailfish collections from the Atlantic ( U.S. proximately 80% of the Atlantic sailfish Cosmopolitan Species With
and Brazil), Pacific (Mexico), and Indian and were separated from ubiquitous clade Discontinuous Distributions
Oceans (Australia) exhibited a range of haplotypes by an average nucleotide se- Conspecific populations of bluefish, Atlan-
within-sample diversities ( Table 1), with quence divergence of 0.65%. A mean nu- tic mackerel, and chub mackerel all exhib-
432 The Journal of Heredity 1998:89(5)the entire mtDNA molecule ( Brown et al.
1979), estimates of divergence times be-
tween conspecific populations in the
North Atlantic range from 5,000 years for
Atlantic mackerel to 130,000 years for
bluefish. Although caution must be used
in the application of divergence times,
these data demonstrate a difference in the
genetic connectivity of Atlantic mackerel,
chub mackerel, and bluefish across the At-
lantic.
Over the past million years the distri-
bution of tropical and temperate water
masses has changed dramatically ( Dans-
gaard et al. 1993; Savin et al. 1975), and
even as recently as 18,000 years ago, dur-
ing the last ice age, temperatures may
have cooled sufficiently in some tropical
areas to allow contact (or colonization) of
isolated populations of temperate fishes
(CLIMAP 1976). The range of genetic di-
vergences among conspecific populations
of cosmopolitan temperate fishes suggests
that there has been multiple opportunities
for contact. Differences in dispersal abili-
ties, or the stochastic nature of dispersal,
could be responsible for the observed
range in divergence times across temper-
ate species. In addition, slight differences
in temperature preferences between spe-
cies, combined with historical tempera-
ture fluctuations, may have presented
some species with a greater opportunity
for gene flow.
Comparisons of patterns of genetic re-
lationships among distant populations of
bluefish and mackerels from other areas
within the Atlantic Ocean were less con-
gruent than those in the North Atlantic
due to the fact that bluefish from the west-
ern South Atlantic ( Brazil) were distantly
related (␦ ⬎ 1.3%) to all other geographi-
cally isolated conspecific populations.
Large divergences were not observed be-
tween other bluefish populations or among
conspecific populations of chub mackerel
within the Atlantic Ocean. A similar phy-
Figure 3. UPGMA clustering of net mean nucleotide sequence divergences (␦) among geographically distant logeographic pattern was not evident for
collections of four ‘‘species’’ of continuously distributed pelagic marine fishes: yellowfin tuna (T. albacares), white chub mackerel in the Atlantic Ocean. Chub
marlin/striped marlin (T. audax/T. albidus), blue marlin(M. nigricans), and sailfish(I. platypterus).
mackerel from Argentina exhibited close
genetic affinities with all other Atlantic
ited close genetic relationships across the quence divergence can be converted to samples ( Table 3), and no significant het-
North Atlantic, although there was a con- estimates of divergence times by the ap- erogeneity was observed in the distribu-
siderable range in genetic affinities among plication of a molecular clock, although it tion of haplotypes between collections
species. Haplotypes were shared among is realized that evolutionary rates may from Argentina and the Ivory Coast. The
conspecific populations of Atlantic mack- vary among and within lineages over time relative isolation of Brazilian bluefish is
erel and chub mackerel, but not among (Avise 1994), and that stochastic variation puzzling and may simply reflect the sto-
bluefish samples, and net nucleotide se- in the accumulation of relatively small chastic nature of long-distance dispersal
quence divergences between conspecific numbers of substitutions may represent a of temperate species across the tropics.
populations of the three species ranged substantial source of error ( Hillis et al. Crosetti et al. (1994) employed RFLP
from 0.01% (Atlantic mackerel) to 0.26% 1996). Using a rate of 2% nucleotide se- analysis of the entire mtDNA genome to
( bluefish) ( Table 3). Values of mtDNA se- quence divergence per million years for study the global phylogeography of grey
Graves • Population Structures of Cosmopolitan Marine Fishes 433Table 3. Comparison of within-ocean net nucleotide sequence divergence (␦) among conspecific gigedo Islands represent the furthest pen-
populations of discontinuously distributed pelagic fishes
etration of the species into the eastern Pa-
Species Populations ␦ cific. The reduction in genetic diversity of
the Revillagigedo Island sample, and its
North Atlantic (west/east)
close affinity to the western Pacific popu-
Bluefish U.S./Portugal 0.26
Atlantic mackerel U.S./England 0.01 lations ( Taiwan and Japan) is consistent
Chub mackerel U.S./Israel (Mediterranean) 0.14 with the interpretation that the Revillagi-
South Atlantic (west/east) gedo Islands population may be the result
Bluefish Brazil/South Africa 1.66 of a recent colonization event.
Chub mackerel Argentina/Ivory Coast 0.03
Argentina/Israel (Mediterranean) 0.07
Argentina/South Africa 0.10 Continuously Distributed Cosmopolitan
Atlantic Ocean (north/south) Fishes
Bluefish U.S./Brazil 1.48 As expected, cosmopolitan marine fishes
Portugal/South Africa 0.35 with continuous distributions exhibited
Chub mackerel U.S./Argentina 0.04
Israel (Mediterranean)/Ivory Coast 0.00 far less genetic structuring than species
Israel (Mediterranean)/South Africa 0.01 with discontinuous distributions (com-
North Pacific (west/east) pare Figures 2 and 3). However, the level
Chub mackerel Japan/U.S. 0.32 of intraspecific structuring within circum-
Spotted chub mackerel Japan/Mexico 0.02 tropical species ranged from a lack of ge-
All values were estimated using RFLP analysis of mtDNA employing 9 to 12 restriction endonucleases. netic differences between ocean popula-
tions to significant but shallow structuring
within an ocean.
mullet (Mugil cephalus), which occurs in ing or after the Pleistocene, suggesting The distribution of mtDNA haplotypes
discontinuous distributions throughout that dispersal events have been an impor- among five samples of yellowfin tuna from
temperate and tropical waters, and re- tant factor in shaping the current genetic geographically distant locations in the Pa-
ported a net nucleotide divergence be- relationships among conspecific popula- cific Ocean was not significantly hetero-
tween eastern and western Atlantic sam- tions. Dispersal could be promoted within geneous, nor was heterogeneity observed
ples of 1.78%. This value is comparable to these temperate species by both larval when a sixth sample from the Atlantic
those between bluefish from Brazil and drift and adult movements. Bluefish are Ocean was included. Ward et al. (1994)
other Atlantic conspecific populations. capable of extended movements ( Lund also found negligible partitioning of mt-
However, genetic divergences between all and Maltezos 1970) and large schools of DNA variation among samples of yellowfin
grey mullet populations were consistently mackerel are encountered well offshore tuna from the Pacific Ocean, although they
larger than those between bluefish (ex- (Collette and Nauen 1983), providing a did report statistically significant differ-
cluding Brazil), chub mackerel, or spotted possible mechanism for dispersal across ences at an allozyme locus between
mackerel populations. This suggests a ocean basins. Within the North Atlantic, pooled western and eastern Pacific sam-
greater time of isolation among grey mul- entrainment of larvae into the Gulf Stream ples.
let populations, and the potential for a dif- could provide a mechanism for transport, Blue marlin, white marlin, and sailfish,
ferent isolating mechanism. as has been suggested for bluefish ( Hare like yellowfin tuna, exhibited a lack of pop-
Close genetic affinities were revealed be- and Cowen 1993). The potential for larval ulation structuring within oceans. For all
tween conspecific populations of spotted transport may be important in other cur- three billfish species, conspecific collec-
chub mackerel and chub mackerel across rent systems as well. tions from geographically distant sites
the North Pacific. Samples of spotted chub The role of dispersal is clearly impor- within an ocean exhibited distributions of
mackerel from Japan and Mexico (two tant for establishing new populations, and mtDNA haplotypes that were not signifi-
haplotypes in common, ␦ ⫽ 0.02%) were the possibility of recent colonization cantly heterogeneous. Therefore, the null
more closely related than chub mackerel events was suggested for populations of hypothesis of a common gene pool could
from Japan and California (no haplotypes bluefish and spotted chub mackerel. In not be disproved. A similar observation
in common, ␦ ⫽ 0.30%). Estimated diver- contrast to other conspecific collections, was reported for swordfish (Xiphias glad-
gence times for the conspecific popula- bluefish samples from eastern Australia ius) in the North Pacific by Grijalva-Chon
tions of the two species are 10,000 years were nearly monotypic, and the haplo- et al. (1994). Their RFLP analysis of mt-
and 150,000 years, respectively. Genetic types present were most closely related to DNA revealed no significant differences
relationships between sardines (Sardinops those in western Australia. These data are among large collections of swordfish from
sagax) across the North Pacific (Japan and consistent with a recent colonization of Mexico, Hawaii, and Japan.
California) based on sequence analysis of eastern Australia by western Australian The lack of significant heterogeneity in
the mitochondrial control region ( Bowen bluefish, most likely via the Great Austra- the distribution of mtDNA haplotypes
and Grant 1997) and cytochrome-b gene lian Bight during a period of elevated wa- among collections of pelagic fishes across
(Grant et al., in press) correspond to an ter temperatures. broad regions is consistent with some
isolation time of a few hundred thousand A similar reduction of variation relative gene flow between geographically distant
years, similar to that estimated for chub to other conspecific populations was not- areas. Theoretically, gene flow on the or-
mackerel across the North Pacific. ed for the spotted chub mackerel sample der of a few individuals per generation
The genetic relationships among con- from Mexico. Spotted chub mackerel do would be sufficient to prevent the accu-
specific populations of bluefish and mack- not occur along the mainland coast of mulation of significant genetic drift be-
erels are consistent with divergences dur- North or South America, and the Revilla- tween geographically distant locations
434 The Journal of Heredity 1998:89(5)( Hartl and Clark 1989). Tagging studies (␦ ⫽ 0.12%) was only twice the maximum idence of a deeper genetic architecture.
have demonstrated the capacity for long- value found between geographically dis- For each of these species, two genetically
range dispersal in many pelagic species tant samples of striped marlin within the distinct mtDNA lineages were present in a
( Hunter et al. 1986; Scott et al. 1990). Cou- Pacific Ocean (␦ ⫽ 0.06%), and lower than geographically restricted area, a pattern
pled with continuous suitable habitat the divergences between conspecific sam- consistent with a period of isolation and
across oceans, and the occurrence of pro- ples of blue marlin and sailfish from the secondary contact (Avise et al. 1987). The
tracted spawning over a broad geographic Atlantic and Pacific Oceans (␦ ⫽ 0.15% average nucleotide sequence divergence
area, the occurrence of some intraocean and 0.27%, respectively). Sequence analy- between haplotypes of the divergent
gene flow does not seem problematic. In sis of the mitochondrial cytochrome-b clades (d ⫽ 0.65–1.34%) suggests an iso-
the case of yellowfin tuna, interocean gene gene by Finnerty and Block (1995) also re- lation event dating to the Pleistocene.
flow would be possible around the Cape vealed a high genetic similarity between The high haplotype diversities and
of Good Hope during the austral summer. white and striped marlin. Together these close genetic similarities among haplo-
The existence of yellowfin tuna and other data suggest that a reexamination of the types observed in cosmopolitan species is
circumtropical species in this area has taxonomic status white marlin and striped consistent with reports for several marine
been demonstrated ( Talbot and Penrith marlin is warranted. fishes (Shields and Gust 1995) and has
1962). Within the Pacific Ocean striped marlin been interpreted as evidence for recent
In contrast to yellowfin tuna, both blue exhibited significant heterogeneity among population expansion (Rogers 1995).
marlin and sailfish exhibited significant ge- geographically distant collections. Although Grant and Bowen (1998) reported high
netic differences between samples from the phylogeographic structuring among haplotype diversities and close genetic re-
the Atlantic and Pacific Oceans. The mt- striped marlin collections was relatively lationships among haplotypes for several
DNA haplotypes of Atlantic collections of shallow ( Figure 3), the data suggest very species of anchovies and sardines. They
each species comprised two genetically limited gene flow among striped marlin suggested that such a pattern could result
divergent lineages, only one of which was from distant areas. This was not expected from periodic extinctions and recoloniza-
represented in Pacific samples. However, as the natural history of the species would tions, likely events for species which oc-
average nucleotide sequence divergence appear conducive to gene flow. Striped cupy upwelling zones that may be geolog-
between ‘‘Atlantic’’ and ‘‘ubiquitous’’ hap- marlin are continuously distributed across ically ephemeral ( Hayward 1997). Such an
lotypes of blue marlin was almost twice the Pacific Ocean, exhibit a protracted explanation cannot account for the phy-
that of sailfish (d ⫽ 1.23% and 0.65%, re- spawning season over a large geographic logeographic pattern found for many of
spectively), and the Atlantic clade of hap- area, and individuals are capable of un- the tropical cosmopolitan species exam-
lotypes was represented in approximately dertaking extensive movements (Squire ined in this study, as tropical marine wa-
80% of Atlantic sailfish, while the Atlantic 1987). The observed spatial partitioning of ters are believed to have been a relatively
clade occurred in less than 40% of Atlantic genetic variation among widely separated constant environment for millions of
blue marlin. Finnerty and Block (1992) collections of striped marlin could be the years, resulting in high species diversities
also noted the presence of two divergent product of ephemeral evolutionary ( Briggs 1974). Other factors must also be
mtDNA lineages in blue marlin based on ‘‘noise’’ due to a large variance in female responsible for the relatively high diver-
their analysis of 26 mitochondrial cyto- reproductive success of these prolific sity and recent coalescence of mtDNA
chrome-b sequences. spawners ( Hedgecock 1994), or it could haplotypes of cosmopolitan marine fishes.
Divergent mtDNA lineages also have result from spawning site fidelity. Distinct
been reported for swordfish in the Atlantic seasonal movements associated with
Implications for Management and
Ocean. Sequence analyses of the sword- spawning have been reported for striped
Conservation
fish mtDNA control region demonstrated marlin off the coast of Mexico (Squire and
the presence of a genetically divergent lin- Suzuki 1990). Effective management and conservation of
eage of mitochondrial haplotypes that was fisheries resources requires an under-
most frequent in swordfish from the Med- Intraspecific Phylogenies standing of the population structure of the
iterranean and occurred at decreasing fre- A range of intraspecific population struc- exploited species, and these studies have
quencies in the samples from the North tures was exhibited by the cosmopolitan provided information to refine existing
Atlantic, South Atlantic, and Pacific, re- fishes investigated in this study, and as ex- management models. In the Atlantic
spectively (Alvarado-Bremer et al. 1996; pected, species with discontinuous distri- Ocean, blue and white marlin are managed
Rosell and Block 1996). butions displayed greater divergence among by the member nations of the Internation-
Based on the phylogeographic structur- geographically distant samples than con- al Commission for the Conservation of At-
ing exhibited between conspecific popu- tinuously distributed fishes. Relative to lantic Tunas ( ICCAT ). Both blue marlin
lations of blue marlin and sailfish from the similar analyses of freshwater fishes or and white marlin are overexploited, and
Atlantic and Pacific Oceans, one would ex- terrestrial organisms, the magnitude of the biomass of each species is less than
pect an even greater genetic divergence population structuring exhibited by pelag- 25% of that necessary to support maxi-
between white marlin and striped marlin. ic marine fishes is extremely small (Avise mum sustainable yield (SCRS 1997). ICCAT
This was not the case ( Figure 3). The two 1994). previously assumed that each species
species shared two mtDNA haplotypes, In general, haplotypes within a species comprised two stocks, north and south of
and genetically divergent mtDNA lineages were closely related, differing by the gain 5⬚N latitude. However, the lack of signifi-
characteristic of Atlantic samples of blue or loss of a few restriction sites. In only cant genetic differences between conspe-
marlin and sailfish were not present in three instances—Australian and New Zea- cific collections of blue marlin and white
white marlin. The net genetic divergence land spotted chub mackerel, Atlantic blue marlin from the North and South Atlantic
between white marlin and striped marlin marlin, and Atlantic sailfish—was there ev- is consistent with the existence of a single
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