Evolution on your dinner plate?
Malin Pinsky Ecology, Evolution, and Natural Resources
Institute of Marine and Coastal Sciences Rutgers University
The raw material for evolution
DNA
The raw material for evolution
DNA
The raw material for evolution
DNA from Mother
from Father
Parts of the genome
Gene or locus
Parts of the genome
Allele
Source of variation
• Mutations
Source of variation
• Mutations
• Germ line copy passed to offspring
Oh cruel herb of soap, Bane of burritos worldwide, The slayer of taste.
from ihatecilantro.com
OR6A2 gene
People with two “soapy” alleles more likely than others (15% vs. 10%) to dislike cilantro
Eriksson et al. 2012 Flavour
Population
Population
Population
Population
• Allele frequencies – 50% blue – 50% red
Phenotype: running speed
Fast Slow
Phenotype: running speed
Fast Slow
Moderate
Population
• Fitness: ability to pass genes on to future generations
Population
• Fitness: ability to pass genes on to future generations
Population
• Fitness: ability to pass genes on to future generations
Population
• Fitness: ability to pass genes on to future generations
33% blue 67% red
Evolution
1. Heritable variation
Evolution
1. Heritable variation 2. More offspring than can survive
Evolution
1. Heritable variation 2. More offspring than can survive 3. Offspring vary in ability to survive
and reproduce
Bighorn sheep
Coltman et al. 2003 Nature
Bighorn sheep
down to thousands might have no effect on heterozygosity,but could result in a decline in allelic diversity [22]. Bycontrast, greater harvest of males through hunting inungulates could have limited effect on allelic diversitywhile reducing heterozygosity because NC (e.g. femalenumbers) can remain large even whenNe is reduced owingto increasingly skewed sex ratios favoring females [33].
The loss of genetic variation will also be influenced bygene flow among subpopulations that comprise a metapo-pulation. Estimating the effective population size of ametapopulation is extremely complex [34]. In addition,harvesting might have unexpected effects on the overallNe of a metapopulation. For example, Hindar and col-leagues have found that small subpopulations within ametapopulation of Atlantic salmon Salmo salar contributemore per spawner to the overall effective population sizethan large subpopulations, and harvesting of the subpopu-lations jointly in mixed-stock fisheries has a relativelylarger demographic effect on small than large populations[35].
Exploitative selectionSelective genetic changes within subpopulations resultingfrom exploitation are inevitable because increasingmortality will result in selection for earlier maturationeven if harvest is independent of phenotype [5]. Moreover,harvesting of wild populations is inevitably phenotypicallynonrandom [5]. That is, individuals of certain phenotypes(e.g. sizes or behaviors) are more likely than others to beremoved from a wild population by harvesting. Such se-lective harvest will bring about genetic changes in har-vested populations if the favored phenotype has at least apartial genetic basis (i.e. is heritable). In addition, suchchanges are likely to reduce both the frequency of desirablephenotypes (Box 2) and productivity.
We use the term ‘exploitative selection’ for the process ofselection resulting from human harvest. The term is ana-logous to ‘artificial selection’ used by Darwin for the inten-tional selection of certain traits in domestic animals andplants. Rapid genetic change in response to strong selec-tion has been called ‘contemporary evolution’ [36]. How-ever, this term can bemisleading because evolution ismorethan just change by natural selection. Thus, loss of geneticvariation caused by genetic drift or increase in geneticvariation caused by hybridization would also representcontemporary evolution.
The rate of genetic change by exploitative selectiondepends upon the amount of additive genetic variationfor the trait (heritability):
R ¼ HNS; [1]
where HN is the narrow-sense heritability, S is theselection differential (the difference in the phenotypicmeans between the selected parents and the whole popu-lation) and R is the response (the difference in thephenotypic means between the progeny generation andthe whole population in the previous generation) [32]. Inthe case of exploitative selection, S will be affected bothby the intensity of harvest (the proportion of the indi-viduals harvested) and the phenotypic selectivity of theharvest.
There aremany examples in the literature of phenotypicchanges in exploited populations thatmight be the result ofexploitative selection (Table 2). However, it has been diffi-cult to determine whether observed phenotypic changesover time indicate genetic change or are caused by otherfactors such as relaxing density-dependent effects ongrowth due to reductions in population density, or abioticfactors such as temperature affecting growth and devel-opment [37]. A recent review in this journal critically
Box 2. Effects of trophy hunting
Trophy hunting (and fishing) targets individuals with certaindesirable phenotypes [66]. The result is increased mortality andreduced fitness of those individuals with desirable phenotypes.Consequently, phenotypes that are considered desirable willdecrease in frequency. For example, populations of bighorn sheepOvis canadensis are often managed to provide a source of large-horned rams for trophy hunting [67]. In one population of bighornsheep at Ram Mountain, Alberta, Canada, a total of 57 rams wereharvested under such an unrestricted management regime over a30 year period [67]. This corresponded to an average harvest rate of"40% of the legal-sized rams in a given year, with the average age ofa ram at harvest of 6 years. Because rams in this population do notgenerally reach their peak reproductive years until 8 years of age[67], hunters imposed an artificial selection pressure on horn sizethat had the potential to bring about genetic change, provided thatthe horn size was heritable.
The heritability of horn size, or any other quantitative trait, can beestimated using pedigree information [60]. Mother–offspring rela-tionships in the Ram Mountain population were known throughobservation, and father–offspring relationships were determinedusing microsatellites for paternity and sibship analyses [67]. An‘animal model’ analysis (named as such because it estimates theexpected genetic ‘breeding value’ [twice the expected deviation ofan individual’s offspring from the term population mean for the traitbeing considered] for each individual animal in the population) wasconducted, which uses relatedness across the entire pedigree toestimate narrow-sense heritability. Horn length was found to behighly heritable (HN = 0.69) [67].
The examination of individual breeding values revealed that ramswith the highest breeding values were harvested earliest (Figure Ia)and therefore had lower fitness than rams of lower breeding value[67]. As a consequence, the average horn length observed in thepopulation has steadily declined (Figure Ib). Unrestricted harvestinghas therefore resulted in a decline in the trait that determines trophyquality (i.e. horn length) by removing desirable rams of high geneticquality before their reproductive peak.
Figure I. (a) Breeding value (twice the expected deviation of an individual’soffspring from the term population mean) for horn length of trophy-harvestedmale bighorn sheep at Ram Mountain. Males with greater breeding value areharvested at a younger age and thus tend to have lower fitness than males withlower breeding value [67]. (b) Plot of mean (#SE) horn length of 4-year-oldrams over a 30 year period showing the decline of mean horn length in thispopulation.
Review Trends in Ecology and Evolution Vol.23 No.6
331
Coltman et al. 2003 Nature
Fisheries effects
1957
Fisheries effects
1957 2007
Importance of diversity in populations
Importance of diversity in populations
• Raw material for evolution
Importance of diversity in populations
• Raw material for evolution
• “Insurance policy”
Importance of diversity in populations
• Raw material for evolution
• “Insurance policy” • Avoid inbreeding
Measuring molecular diversity
• Number of alleles
Measuring molecular diversity
• Number of alleles • Heterozygosity
– probability of picking two different alleles
Genetic bottlenecks
Alleles: 3 Heterozygosity: 60%
Genetic bottlenecks
Alleles: 3 Heterozygosity: 60%
Alleles: 2 Heterozygosity: 40%
Bottleneck examples
Robert Schwemmer
Northern elephant seal
Florida panther
Can fisheries cause bottlenecks?
Tuna, billfishes, swordfish Myers & Worm 2003 Nature
Purse seiner for salmon
Can fisheries cause bottlenecks?
Collapsed populations still abundant!
Num
ber o
f alle
les
(Ā) 12
11
10
9
8
71940 1960 1980 2000
A few examples?
New Zealand snapper (Pagrus auratus) after Hauser et al. 2002 PNAS
Peter Halasz
Num
ber o
f alle
les
(Ā) 12
11
10
9
8
71940 1960 1980 2000
A few examples?
Also: – Atlantic
cod – European
plaice
New Zealand snapper (Pagrus auratus) after Hauser et al. 2002 PNAS
Peter Halasz
Num
ber o
f alle
les
(Ā) 12
11
10
9
8
71940 1960 1980 2000
A few examples?
Also: – Atlantic
cod – European
plaice
But not: – Atlantic
cod – Bluefin
tuna – Canary
rockfish
New Zealand snapper (Pagrus auratus) after Hauser et al. 2002 PNAS
Peter Halasz
Data
• Microsatellite diversity – 202 studies of 140 species
Available online at www.sciencedirect.com
Fisheries Research 89 (2008) 196–209
Stock identity of horse mackerel (Trachurus trachurus) in the Northeast
Atlantic and Mediterranean Sea: Integrating the results from
different stock identification approaches
P. Abaunza a,∗, A.G. Murta b, N. Campbell c, R. Cimmaruta d, A.S. Comesana e, G. Dahle f,
M.T. Garcıa Santamarıa g, L.S. Gordo h, S.A. Iversen f, K. MacKenzie c, A. Magoulas i,
S. Mattiucci j, J. Molloy k, G. Nascetti d, A.L. Pinto b, R. Quinta b, P. Ramos b,
A. Sanjuan e, A.T. Santos b, C. Stransky l, C. Zimmermann m
a Instituto Espanol de Oceanografıa, P.O. Box 240, 39080 Santander, Spain
b Instituto de Investigacao das Pescas e do Mar, Av. Brasilia, 1400 Lisboa, Portugal
c School of Biological Sciences (Zoology), The University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
d Department of Ecology and Sustainable Economic Development, Tuscia University, Via S. Giovanni Decollato, 1, 01100 Viterbo, Italy
e Facultade de Bioloxıa, Edificio de Ciencias, Universidade de Vigo, E-36200 Vigo, Spain
f Institute of Marine Research, P.O. Box 1870, Nordnes, N-5817 Bergen, Norway
g Instituto Espanol de Oceanografıa, Avda. Tres de Mayo 73, 38005 Santa Cruz de Tenerife, Spain
h Facultade de Ciencias de Lisboa (IO/DBA), Bloco C-2, Campo Grande, 1749-016 Lisboa, Portugal
i Hellenic Centre for Marine Research, Institute of Marine Biology and Genetics, P.O. Box 2214, GR 710 013 Iraklio, Greece
j Department of Public Health Sciences, Section of Parasitology, “Sapienza” University of Rome, piazzale Aldo Moro n◦ 5, 00185 Rome, Italy
k The Marine Institute, Parkmore Industrial Estate, Galway, Ireland
l Bundesforschungsanstalt fur Fischerei, Institut fur Seefischerei, Palmaille 9, D-22767 Hamburg, Germany
m Bundesforschungsanstalt fur Fischerei, Institut fur Ostseefischerei, Alter Hafen Su 2, D-18069 Rostock, Germany
AbstractHorse mackerel stock identification was carried out with the aim of obtaining management units that were meaningful biological entities and
thus improving the management of the resource. The stock identification was made by integrating both established and innovative approaches such
as genetic markers (allozymes, mitochondrial DNA, microsatellite DNA and SSCP on nuclear DNA), morphometry, parasites as biological tags,
and life history traits (growth, reproduction and distribution), within the EU-funded HOMSIR project. The sampling covered almost the whole
distribution range of horse mackerel through 20 sampling localities in Northeast Atlantic and Mediterranean Sea. Horse mackerel showed low
levels of genetic differentiation, stable genetic structure over the study time and high levels of genetic variability. However, several approaches
(morphometrics and parasites) support the separation between the Atlantic Ocean and the Mediterranean Sea in horse mackerel populations,
although the most western Mediterranean area could also be mixed with the Atlantic populations. In the Northeast Atlantic, various stocks can be
distinguished mainly based on morphometrics, parasites and life history traits: a “southern” stock is distributed along the West Atlantic coast of
the Iberian Peninsula south to Cape Finisterre (NW Spain); a “western” stock, along the west coast of Europe from Cape Finisterre to Norway and
the “North Sea” stock. These results implied the revision of the boundaries of the southern and western stocks as previously defined. Results also
suggested that adult horse mackerel could migrate through different areas following the west coasts in the Northeast Atlantic (i.e. between Celtic
Seas and northern North Sea). Horse mackerel from the Mauritanian coast is distinguished by its high growth rate and high batch fecundity. Based
on the results from morphometric analysis and the use of parasites as biological tags, the horse mackerel population in the Mediterranean Sea is
sub-structured into at least three main areas: western, central and eastern Mediterranean. In this contribution, we have integrated the fundamental
findings of different approaches showing that the holistic approach is the appropriate way to identify horse mackerel stocks, on covering multiple
aspects of the biology of the species and reducing the type I error in stock identification.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Trachurus trachurus; Stock identity; Holistic approach; Northeast Atlantic; Mediterranean Sea; Natural marks; Life history traits
∗ Corresponding author. Tel.: +34 942291060; fax: +34 942275072.
E-mail address: [email protected] (P. Abaunza).
0165-7836/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.fishres.2007.09.022
Spatio-temporal populationstructuring and genetic
diversity retention in depleted Atlantic Bluefin tuna
of the Mediterranean Sea
Giulia Riccionia,1, Monica Landi
b,1,2, Giorgia Ferrarab, Ilaria Milano
b, Alessia Carianib, Lorenzo Zane
c, Massimo Sellad,3,
Guido Barbujania, and Fausto Tinti
b,4
aDepartment of Biologyand Evolution, Univ
ersity of Ferrara, 44100 Ferrara, Italy;
bDepartment of Experimental Evolution
ary Biology, University of Bologna,
40126 Bologna, Italy;cDepartment of Biology,
University of Padova, 35121 Padova, Italy; a
nd dInstitute Center for Marine Research, 52210 Rovinj, Croatia
(formerly Istituto Italo-Germanico di Biologia Marina/Deutsch-Italienisches Ins
titut für Meersbiologie, Rovigno, Italy)
Edited by Barbara Block, StanfordUniversity, Stan
ford, CA, and accepted by the Editorial BoardDecember 1, 2009 (received for review July 24, 2009)
Fishery genetics have greatly changed our understandingof
population dynamics and structuring in marine fish. In this study,
we show that theAtlantic Bluefin tuna (ABFT, Thu
nnus thynnus),an
oceanic predatory species exhibiting highly migratory behavior,
large population size, and high potential for dispersal during
early
life stages, displays significant ge
netic differences over space and
time, both at the fine and large scales of variation. We compared
microsatellite variationof contem
porary (n=256) andhistorical (n=
99) biological samples of ABFTs of the central-western Mediterra-
nean Sea, the latter dating back to the early 20th century.Measures
of genetic differentiationand a general hetero
zygote deficit sug-
gest that differences exist among population samples, both now
and 96–80 years ago. Thus, ABFTs do not represent a
single panmic-
tic population in theMediterranean Sea. Statistics designed to infer
changes in population size, both from current and past genetic var-
iation, suggest that some Mediterranean ABFT populations,
although still not severely reduced in their genetic po
tential, might
have suffered fromdemographic declines. The short-te
rmestimates
of effectivepopulation sizeare straddle
don theminimumthreshold
(effectivepopulationsize=500) indicatedt
omaintaingeneticdiver-
sity and evolutionary potential across several generations in
natural populations.
ancient DNA | effective population size | genetic structure | large pelagic
fishes | Thunnus thynnus
With an impressive amount of data accumulated in the last
10–15 years, genetic studies have greatly changed our
understanding of the ecology and evolution of marine fish pop-
ulations by showing evidence of complex genetic struc
ture at the
spatial and temporal scales of variation. This is esp
ecially true for
fish species with high mobility, high potential for dispersal during
egg and larval stages, andlarge population sizes (1, 2). Accurate
estimates of genetic variation in fish populations, both
for neutral
and adaptive loci, can also suggest unique strategies for stock
management and conservation of evolutionary potential in
severely exploited fishery resources (3–5). The assessment of
population dynamics, environmentally driven changes, and levels
of exploitation in large pelagic fish is crucial for bothstock man-
agement and conservation of marine ecosystems dominated by
these oceanic toppredators (6). Although fisheries s
till remain the
chief source of data for assessing spatiotemporal population
dynamics of these fish (7–10), wheneverpossible, their findings
shouldbe comparedwith thoseoffishery-independ
ent approaches,
such as genetic, electronic, andmicrochemical tagging experi
ments
(11–13), to have more accurate data on the key features of pop-
ulation dynamics, such as spawning and migrations (10).
The Atlantic Bluefin tuna (ABFT, Thunnus thynnus) is a large
top-predator fishexploiting the pelagic ecosystems of the North
Atlantic Ocean andMediterranean Sea.Much like the other
large
tunas, the ABFT displays highly migratory behavior, with docu-
mented transoceanic andlarge-scale movements for feeding and
reproduction, high fecundity, and high mortality of larval stages
(reviewed in 14, 15). Nonetheless, tagging experiments and fish-
ery data analyses have unraveled an unexpected and complex
interplay of ecological, behavioral,
and reproductive factors that
could affect the spatial and temporal populationdynamics at the
large scale (11, 16). Microchemical signatures in otoliths of
yearlings (i.e., young-of-the-year) unequivocally identified two
main spawning areas [i.e., the Mediterranean Sea for the Easte
rn
Atlantic population, the Gulf of Mexico for the Western Atlantic
population (13)]. Because of high rates of natal homing of
spawning adults to their native areas (95.8% for the Medi-
terranean Sea and 99.3% for the Gulf of Mexico) and limited and
more complex movements in sexually mature ABFTs (11, 17), the
two populations show significant genetic divergence at both
microsatellite (12) and mtDNA (18) loci. The two ABFT pop-
ulations differ insize, with the eastern population approximately
10 times as large as the western population (19). Both are suf-
fering from overfishing and are considered depleted, consistent
with the continuous decline of the spawning stock biomass
(which, in the eastern stock, is now at 40% of the 1970s levels),
with the high fishing mortality rate of age class 8 and older indi-
viduals, and with modeling predictions (16, 19, 20).
The complex population dynamics exhibited by ABFTs at the
large scale is also apparent at a finer scale in the Mediterranean
Sea (16). Size-dependent movements and spawning in different
areas and periods have been documented (15, 21–23). Genetic
variation among three geographical samples suggested that at
least two subpopulations inhabit and persist over short time
periods (3 years) in the western and eastern Mediterranean Sea,
yielding Wright’s genetic variance (FST) values within the Med-
iterranean Sea between 0.0007 and 0.0087 (12, 24). In this study,
we started from a more thorough sampling of Mediterranean
ABFTs in space and time. Along with an extensive spatial sam-
pling of contemporary ABFTs carried out from 1999 to 2007 in
the central-western Mediterranean (CWM), we also had access
to historical ABFT specimens collected by one of the authors
(M.S.) in the CWM tuna traps between 1911 and 1926 (Fig. S1).
Author contributions: M.L., G.B, and F.T. designed research; M.L., G.F., I.M., A.C., and M.S.
performed research; G.R.,M.L., G.F., and L.Z. analyzed data; and G.R., G.F., L.Z.,
G.B, and
F.T. wrote the paper.
The authors declareno conflict of inte
rest.
This article is a PNAS Direct Submission. B.B. is a guest editor inv
ited by the Editorial Board.
1G.R. and M.L. contributedequally to this work.
2Present address: Department of Biology,
University of Minho, Campus de Gualtar, 4710–
057 Braga, Portugal.
3Deceased April 9, 1959.
4To whom correspondenceshould be addressed at: Department of Experim
ental Evolu-
tionary Biology, University of Bologna, via
Selmi 3, 40126 Bologna, Italy.E-mail: fausto.
This article contains supporting information online at www.pnas.org/cgi/content/full/
0908281107/DCSupplemental.
2102–2107 | PNAS | February 2, 2010 | vol. 107 | no. 5
www.pnas.org/cgi/doi/10.1073/pnas.
0908281107
TECHNICAL NOTE
Isolation and characterization of microsatellite markers
for the heavily exploited rockfish Sebastes schlegeli,
and cross-species amplification in four related Sebastes spp.
Hye Suck An Æ Jung Youn Park Æ Mi-Jung Kim Æ
Eun Young Lee Æ Kyung Kil Kim
Received: 19 February 2009 / Accepted: 24 February 2009 / Published online: 7 March 2009
! Springer Science+Business Media B.V. 2009
Abstract Here we report development and characteriza-
tion of 14 polymorphic microsatellite loci from Sebastes
schlegel. Polymorphism at these loci revealed from 3 to 23
alleles. The observed heterozygosity ranged from 0.34 to
1.00, and the expected heterozygosity ranged from 0.31 to
0.95. No linkage disequibrium was found. Two loci were
significantly deviated from HWE (P\ 0.01). The 14 loci
were also surveyed in four other Sebastes species and 12
loci successfully amplified, where allelic diversity ranged
from highly polymorphic to monomorphic. These results
demonstrate these microsatellite markers can be used for
the study of intra- and inter-specific genetic diversity.
Keywords Sebastes schlegel ! Rockfish !
Microsatellites markers ! Cross-amplification
Introduction
Rockfish Sebastes schlegeli, belonging to the family
Sebastinae and an important commercial fish in Korea, is
one of the species for which artificial reproduction and
cultivation have intensively been made throughout Korean
coastal areas to increase the harvest yield since the early
1990s. A stock enhancement program through the release
of hatchery-raised juveniles into natural environments has
been practiced since the middle 1990s. In 2007, approxi-
mately two million seeds were released. In stock
enhancement programs, the genetic characterization of the
stocking species used should be assessed in view of
elucidating and monitoring the effect of such activities on
wild stocks (FAO 1993). Therefore, in recent years, the
extent of stocking impacts upon indigenous populations has
been a focus of attention from viewpoints of conservation
and management for this species. However, to date little is
known about genetic diversity and population differentia-
tion of this species. Information regarding population
structure, levels of geneflow and genetic diversity within
and among populations of species harvested for com-
mercial purposes can provide useful information for
developing conservation and management plans.
Although six microsatellite markers from S. schlegeli
have been already reported by Yoshida et al. (2005), a set
of molecular markers are needed for various other appli-
cations, from further population studies to pedigree
analysis. In this work, we isolated 14 novel microsatellite
markers from S. schlegeli, and represented their evaluation
for cross-species amplification in four other related con-
generic species.
We developed a partial genomic library enriched for CA
repeats as described in the protocol of Hamilton et al.
(1999) with a slight modification using prehybridization
PCR amplification (Gardner et al. 1999). Genomic DNA
was extracted from each fin tissue sample of S. schlegel
captured in western coast of Korea using TNES-Urea
buffer method (Asahida et al. 1996). DNA was simulta-
neously digested with restriction enzymes AluI, RsaI, NheI
and HhaI (New England Biolabs, Bervery, MA, USA).
DNA fragments ranging from 300 to 800 bp were isolated
and ligated to double-stranded linker-adapted primers
(SNX/SNX rev linker sequences). Linker-ligated DNA
fragments were then amplified using single-stranded linker-
adapted primer (SNX) as polymerase chain reaction
primer. Biotinylated dinucleotide repeat sequences [50-
(CA)12GCTTGA-biotin (Li et al. 2002)] were hyb
ridized toH. S. An (&) ! J. Y. Park ! M.-J. Kim ! E. Y. Lee ! K. K. Kim
Biotechnology Research Institute, National Fisheries Research
and Development Institute, Busan 619-705, Korea
e-mail: [email protected]
123
Conserv Genet (2009) 10:1969–1972
DOI 10.1007/s10592-009-9870-8
Demogr
aphic his
tory, g
eograp
hical d
istrib
ution
andrep
roduct
ive
isolat
ionof
distin
ctline
ages of
blue roc
kfish (Se
bastes
mystinu
s),
a marine
fishwith
a high dis
persal
potent
ial
M. O. B
URFO
RD
Departm
entof E
cology
andEvo
lutiona
ry Biolo
gy,Un
iversity
of Calif
ornia San
ta Cruz, S
anta Cru
z, CA,
USA
Introd
uction
Conte
mporary
andevo
lution
arytim
e-scal
e factor
s such
ascur
rent or
wind
patter
ns,geo
graphi
calbar
riers,
demogr
aphic
charac
teristi
cs,phy
sical cha
nges in
the
enviro
nment
, or a
combin
ation of
these
factor
s can
act
tored
ucegen
e flowam
ongpop
ulation
s throug
hout a
specie
s’ rang
e (Avise,
1994).
Inmarin
e system
s, redu
c-
tionor
elimina
tionin
gene flow
maylea
d togen
etic
differe
ntiatio
n orspe
ciation
even wit
hinspe
cies wit
h
long p
elagic
stages
, espec
ially if
popula
tions ar
e separ
ated
into diff
erent
ecolog
ical re
gions.
Select
ivefor
cescan
also
lead to
genetic
structu
reor
specia
tionin
marine tax
a
with a lon
g pelagi
c stage
only if i
t isstro
ngeno
ughto
counte
ract the
homoge
nizing
effect
ofgen
e flow. T
he
evalua
tionof t
hegen
eticrela
tionshi
p among
popula
tions
ordis
tinct
lineage
s inare
aswh
erediv
ergent
lineage
s
overlap
andwh
ereonl
y one
lineage
is foun
d can
improve
ourun
dersta
nding
of the
evolut
ionary
forces
andeve
nts
causin
gspe
ciation
inthe
marine
enviro
nment
. For
example
, high
potent
ialdis
persal
maynot
transl
ateto
high lev
elsof
realize
d gene flow
. We mayalso
gain
insigh
t into
why
there
ishig
hspe
cies div
ersity
in
taxono
mic grou
pswit
h high dis
persal
potent
ial.
Althou
ghthe
rockfis
hes(Sc
orpaen
idae:
Sebaste
s)are
consid
ered a
n ancien
t speci
es flock
(John
s &Av
ise,199
8)
with a hig
h potent
ialfor
disper
sal(th
rough
a pelagi
c
stage
lasting
2–5mont
hs;Lov
e et al.,
2002),
there
is
eviden
ceof
recent
specia
tionwit
hinthe
genus.
Rocha
-
Olivar
eset a
l. (199
9a)fou
ndrec
entspe
ciation
betwe
en
sister-
taxa in
thesub
genus
Sebasto
mus. T
woinv
estiga
-
tions wit
hinroc
kfish
specie
s found
cryptic
specia
tion
within
vermilio
n rockfis
h (Sebas
tesmin
iatus)
that wa
s
caused
bydiff
erence
indep
thdis
tributi
on(Hy
deet a
l.,
2008)
anda sim
ilarpat
tern of
sympat
ricdis
tributi
onof
distin
ctgen
eticpop
ulation
s ofPac
ificoce
anper
ch
Corresp
ondenc
e: Mart
haO.
Burfo
rd,208
Fernow
Hall, C
ornell
Unive
rsity,
Ithaca
, NY 148
53,US
A.
Tel.: +
1 831419
7586; f
ax:+1
831459
3383; e
-mail:
mob8@c
ornell.
edu
ª 2 009
THE AU
THOR . J
. EVO
L .B I O
L .2 2
( 2 00 9
) 14 7
1 –1 4
86
JOURNAL
COMP I LA T
I ON ª 2009
EUROPE
ANSO
C I E TY FO
R EVOLU
T IONAR
Y B IO LOGY
1471
Keywor
ds:
admixtu
re;
assign
menttes
t;
microsat
ellite loc
i;
mismatc
h distrib
ution;
mtDNA con
trol re
gion;
popula
tionexp
ansion
;
reprod
uctive
isolati
on;
specia
tion.
Abstr
act
Under
standi
ngthe
barrier
s togen
eticexc
hange
in taxono
mic grou
ps that
have
a high dis
persal
potent
ialwil
l prov
idecrit
ical in
formatio
n onspe
ciation
in
genera
l. Blue
rockfis
h (Sebas
tesmy
stinus)
aregoo
d taxa to
examine
specia
tion
becaus
e they are
nonmigra
tory inh
abitan
tsof
shallow
rocky
reef hab
itats
along
theeas
tern No
rthPac
ificwit
h a pela
giclarv
al stag
e lastin
g 3–5
months.
Thegoa
l ofthi
s study
was to
analyse
theevo
lution
aryhis
tory a
nddis
tributi
on
patter
nsof
differe
ntline
ages w
ithin
S. mysti
nusdes
cribed
previo
usly and
use
this in
formatio
n toun
dersta
ndthe
specia
tionpro
cess in
this g
roup of
high
disper
salfish
. Themole
cular
data der
ived fro
mspe
cimens
sample
d over
approx
imately
1650 km
ofthe
S.my
stinus
range
reveal
eda nor
therly
and
southe
rlydis
tributi
onfor
thetwo
lineage
s. Almost
equal f
requen
cies o
f both
lineage
s occurr
edat
centra
llyloc
ated sam
pleloc
ations,
with evi
dence
of
reprod
uctive
isolati
onbet
ween
theline
ages. A
demogr
aphic a
nalysis
showe
d
that th
e two line
ages d
iverge
d andexp
erience
d sudden
expans
ionpri
orto the
lastgla
cial maxi
mum, wh
ichaffe
cted
theobs
erved
patter
nof
genetic
structu
re.The
spatial
distrib
ution,
demogr
aphic h
istory
anddeg
reeof g
enetic
distin
ctivene
ss foun
d from
thegen
eticana
lysis, d
espite
thehig
h potent
ialfor
disper
salin
S. mysti
nus, su
ggest b
othline
ages d
iverge
d inallo
patry.
doi: 10
.1111/
j.1420-
9101.2
009.01
760.x
Mar BiolDOI 10.1007/s00227-010-1419-3
123
ORIGINAL PAPER
Life history, ecology and the biogeography of strong genetic breaks among 15 species of PaciWc rockWsh, SebastesArjun Sivasundar · Stephen R. Palumbi
Received: 15 April 2009 / Accepted: 2 March 2010© Springer-Verlag 2010
Abstract Strong genetic change over short spatial scalesis surprising among marine species with high dispersalpotential. Concordant breaks among several species signalsa role for geographic barriers to dispersal. Along the coastof California, such breaks have not been seen across thebiogeographic barrier of Point Conception, but other poten-tial geographic boundaries have been surveyed less often.We tested for strong-population structure in 11 species ofSebastes sampled across two regions containing potentialdispersal barriers, and conducted a meta-analysis includingfour additional species. We show two strong breaks northof Monterey Bay, spanning an oceanographic gradient andan upwelling jet. Moderate genetic structure is just as com-mon in the north as it is in the south, across the biogeo-graphic break at Point Conception. Gene Xow is generallyhigher among deep-water species, but these conclusions areconfounded by phylogeny. Species in the subgenus Sebast-osomus have higher structure than those in the subgenusPteropodus, despite having larvae with longer pelagicphases. DiVerences in settlement behavior in the face ofocean currents might help explain these diVerences. Acrosssimilar species across the same coastal environment, we
document a wide variety of patterns in gene Xow, suggest-ing that interaction of individual species traits such assettlement behavior with environmental factors such asoceanography can strongly impact population structure.
Introduction
For many marine species, larval dispersal is a critical partof migration ability, and life history diVerences betweenspecies can dramatically aVect gene Xow. Investigations ofgenetic diVerences among marine populations have beenwidely used to gauge levels of dispersal, which often scalewith larval traits such as pelagic duration (e.g. Berger 1973;Bohonak 1999; Marko 2004). Species for which larvalduration is short or absent have often been found to havestrong genetic structure among invertebrates (McMillanet al. 1992; Hellberg 1994, 1996) and Wshes (e.g. Waples1987; Doherty et al. 1995; Riginos 2001; Purcell et al.2006). However, unexpectedly strong structure has alsobeen demonstrated for some species that are presumed tohave long distance dispersal potential (e.g. Reeb et al.2000; Barber et al. 2002; Burford and Bernardi 2008).Uncovering the reasons for strong genetic breaks in suchspecies can potentially reveal a great deal about larvalmechanisms that limit dispersal.Some of the clearest explanations of strong geneticbreaks derive from the observation that in some cases, thesebreaks are concordant with strong biogeographic bound-aries. Taxa as diverse as coastal birds, tortoises, Wsh andinvertebrates show strong geographic diVerentiation alongthe southeastern coast of the United States (Avise 1992,1996). Other cases of the conXuence of genetic and biogeo-graphic breaks in the oceans have been found in Indonesia,the western Mediterranean, the East PaciWc and the Red Sea
Communicated by M. I. Taylor.A. Sivasundar · S. R. PalumbiDepartment of Biological Sciences, Hopkins Marine Station, Stanford University, 120 Oceanview Boulevard, PaciWc Grove, CA 93950, USA
A. Sivasundar (&)Division of Aquatic Ecology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012 Bern, Switzerlande-mail: [email protected]
National Oceanic and Atmospheric Administration
Data
• Microsatellite diversity – 202 studies of 140 species
– Number of alleles (A)
Available online at www.sciencedirect.com
Fisheries Research 89 (2008) 196–209
Stock identity of horse mackerel (Trachurus trachurus) in the Northeast
Atlantic and Mediterranean Sea: Integrating the results from
different stock identification approaches
P. Abaunza a,∗, A.G. Murta b, N. Campbell c, R. Cimmaruta d, A.S. Comesana e, G. Dahle f,
M.T. Garcıa Santamarıa g, L.S. Gordo h, S.A. Iversen f, K. MacKenzie c, A. Magoulas i,
S. Mattiucci j, J. Molloy k, G. Nascetti d, A.L. Pinto b, R. Quinta b, P. Ramos b,
A. Sanjuan e, A.T. Santos b, C. Stransky l, C. Zimmermann m
a Instituto Espanol de Oceanografıa, P.O. Box 240, 39080 Santander, Spain
b Instituto de Investigacao das Pescas e do Mar, Av. Brasilia, 1400 Lisboa, Portugal
c School of Biological Sciences (Zoology), The University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
d Department of Ecology and Sustainable Economic Development, Tuscia University, Via S. Giovanni Decollato, 1, 01100 Viterbo, Italy
e Facultade de Bioloxıa, Edificio de Ciencias, Universidade de Vigo, E-36200 Vigo, Spain
f Institute of Marine Research, P.O. Box 1870, Nordnes, N-5817 Bergen, Norway
g Instituto Espanol de Oceanografıa, Avda. Tres de Mayo 73, 38005 Santa Cruz de Tenerife, Spain
h Facultade de Ciencias de Lisboa (IO/DBA), Bloco C-2, Campo Grande, 1749-016 Lisboa, Portugal
i Hellenic Centre for Marine Research, Institute of Marine Biology and Genetics, P.O. Box 2214, GR 710 013 Iraklio, Greece
j Department of Public Health Sciences, Section of Parasitology, “Sapienza” University of Rome, piazzale Aldo Moro n◦ 5, 00185 Rome, Italy
k The Marine Institute, Parkmore Industrial Estate, Galway, Ireland
l Bundesforschungsanstalt fur Fischerei, Institut fur Seefischerei, Palmaille 9, D-22767 Hamburg, Germany
m Bundesforschungsanstalt fur Fischerei, Institut fur Ostseefischerei, Alter Hafen Su 2, D-18069 Rostock, Germany
AbstractHorse mackerel stock identification was carried out with the aim of obtaining management units that were meaningful biological entities and
thus improving the management of the resource. The stock identification was made by integrating both established and innovative approaches such
as genetic markers (allozymes, mitochondrial DNA, microsatellite DNA and SSCP on nuclear DNA), morphometry, parasites as biological tags,
and life history traits (growth, reproduction and distribution), within the EU-funded HOMSIR project. The sampling covered almost the whole
distribution range of horse mackerel through 20 sampling localities in Northeast Atlantic and Mediterranean Sea. Horse mackerel showed low
levels of genetic differentiation, stable genetic structure over the study time and high levels of genetic variability. However, several approaches
(morphometrics and parasites) support the separation between the Atlantic Ocean and the Mediterranean Sea in horse mackerel populations,
although the most western Mediterranean area could also be mixed with the Atlantic populations. In the Northeast Atlantic, various stocks can be
distinguished mainly based on morphometrics, parasites and life history traits: a “southern” stock is distributed along the West Atlantic coast of
the Iberian Peninsula south to Cape Finisterre (NW Spain); a “western” stock, along the west coast of Europe from Cape Finisterre to Norway and
the “North Sea” stock. These results implied the revision of the boundaries of the southern and western stocks as previously defined. Results also
suggested that adult horse mackerel could migrate through different areas following the west coasts in the Northeast Atlantic (i.e. between Celtic
Seas and northern North Sea). Horse mackerel from the Mauritanian coast is distinguished by its high growth rate and high batch fecundity. Based
on the results from morphometric analysis and the use of parasites as biological tags, the horse mackerel population in the Mediterranean Sea is
sub-structured into at least three main areas: western, central and eastern Mediterranean. In this contribution, we have integrated the fundamental
findings of different approaches showing that the holistic approach is the appropriate way to identify horse mackerel stocks, on covering multiple
aspects of the biology of the species and reducing the type I error in stock identification.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Trachurus trachurus; Stock identity; Holistic approach; Northeast Atlantic; Mediterranean Sea; Natural marks; Life history traits
∗ Corresponding author. Tel.: +34 942291060; fax: +34 942275072.
E-mail address: [email protected] (P. Abaunza).
0165-7836/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.fishres.2007.09.022
Spatio-temporal populationstructuring and genetic
diversity retention in depleted Atlantic Bluefin tuna
of the Mediterranean Sea
Giulia Riccionia,1, Monica Landi
b,1,2, Giorgia Ferrarab, Ilaria Milano
b, Alessia Carianib, Lorenzo Zane
c, Massimo Sellad,3,
Guido Barbujania, and Fausto Tinti
b,4
aDepartment of Biologyand Evolution, Univ
ersity of Ferrara, 44100 Ferrara, Italy;
bDepartment of Experimental Evolution
ary Biology, University of Bologna,
40126 Bologna, Italy;cDepartment of Biology,
University of Padova, 35121 Padova, Italy; a
nd dInstitute Center for Marine Research, 52210 Rovinj, Croatia
(formerly Istituto Italo-Germanico di Biologia Marina/Deutsch-Italienisches Ins
titut für Meersbiologie, Rovigno, Italy)
Edited by Barbara Block, StanfordUniversity, Stan
ford, CA, and accepted by the Editorial BoardDecember 1, 2009 (received for review July 24, 2009)
Fishery genetics have greatly changed our understandingof
population dynamics and structuring in marine fish. In this study,
we show that theAtlantic Bluefin tuna (ABFT, Thu
nnus thynnus),an
oceanic predatory species exhibiting highly migratory behavior,
large population size, and high potential for dispersal during
early
life stages, displays significant ge
netic differences over space and
time, both at the fine and large scales of variation. We compared
microsatellite variationof contem
porary (n=256) andhistorical (n=
99) biological samples of ABFTs of the central-western Mediterra-
nean Sea, the latter dating back to the early 20th century.Measures
of genetic differentiationand a general hetero
zygote deficit sug-
gest that differences exist among population samples, both now
and 96–80 years ago. Thus, ABFTs do not represent a
single panmic-
tic population in theMediterranean Sea. Statistics designed to infer
changes in population size, both from current and past genetic var-
iation, suggest that some Mediterranean ABFT populations,
although still not severely reduced in their genetic po
tential, might
have suffered fromdemographic declines. The short-te
rmestimates
of effectivepopulation sizeare straddle
don theminimumthreshold
(effectivepopulationsize=500) indicatedt
omaintaingeneticdiver-
sity and evolutionary potential across several generations in
natural populations.
ancient DNA | effective population size | genetic structure | large pelagic
fishes | Thunnus thynnus
With an impressive amount of data accumulated in the last
10–15 years, genetic studies have greatly changed our
understanding of the ecology and evolution of marine fish pop-
ulations by showing evidence of complex genetic struc
ture at the
spatial and temporal scales of variation. This is esp
ecially true for
fish species with high mobility, high potential for dispersal during
egg and larval stages, andlarge population sizes (1, 2). Accurate
estimates of genetic variation in fish populations, both
for neutral
and adaptive loci, can also suggest unique strategies for stock
management and conservation of evolutionary potential in
severely exploited fishery resources (3–5). The assessment of
population dynamics, environmentally driven changes, and levels
of exploitation in large pelagic fish is crucial for bothstock man-
agement and conservation of marine ecosystems dominated by
these oceanic toppredators (6). Although fisheries s
till remain the
chief source of data for assessing spatiotemporal population
dynamics of these fish (7–10), wheneverpossible, their findings
shouldbe comparedwith thoseoffishery-independ
ent approaches,
such as genetic, electronic, andmicrochemical tagging experi
ments
(11–13), to have more accurate data on the key features of pop-
ulation dynamics, such as spawning and migrations (10).
The Atlantic Bluefin tuna (ABFT, Thunnus thynnus) is a large
top-predator fishexploiting the pelagic ecosystems of the North
Atlantic Ocean andMediterranean Sea.Much like the other
large
tunas, the ABFT displays highly migratory behavior, with docu-
mented transoceanic andlarge-scale movements for feeding and
reproduction, high fecundity, and high mortality of larval stages
(reviewed in 14, 15). Nonetheless, tagging experiments and fish-
ery data analyses have unraveled an unexpected and complex
interplay of ecological, behavioral,
and reproductive factors that
could affect the spatial and temporal populationdynamics at the
large scale (11, 16). Microchemical signatures in otoliths of
yearlings (i.e., young-of-the-year) unequivocally identified two
main spawning areas [i.e., the Mediterranean Sea for the Easte
rn
Atlantic population, the Gulf of Mexico for the Western Atlantic
population (13)]. Because of high rates of natal homing of
spawning adults to their native areas (95.8% for the Medi-
terranean Sea and 99.3% for the Gulf of Mexico) and limited and
more complex movements in sexually mature ABFTs (11, 17), the
two populations show significant genetic divergence at both
microsatellite (12) and mtDNA (18) loci. The two ABFT pop-
ulations differ insize, with the eastern population approximately
10 times as large as the western population (19). Both are suf-
fering from overfishing and are considered depleted, consistent
with the continuous decline of the spawning stock biomass
(which, in the eastern stock, is now at 40% of the 1970s levels),
with the high fishing mortality rate of age class 8 and older indi-
viduals, and with modeling predictions (16, 19, 20).
The complex population dynamics exhibited by ABFTs at the
large scale is also apparent at a finer scale in the Mediterranean
Sea (16). Size-dependent movements and spawning in different
areas and periods have been documented (15, 21–23). Genetic
variation among three geographical samples suggested that at
least two subpopulations inhabit and persist over short time
periods (3 years) in the western and eastern Mediterranean Sea,
yielding Wright’s genetic variance (FST) values within the Med-
iterranean Sea between 0.0007 and 0.0087 (12, 24). In this study,
we started from a more thorough sampling of Mediterranean
ABFTs in space and time. Along with an extensive spatial sam-
pling of contemporary ABFTs carried out from 1999 to 2007 in
the central-western Mediterranean (CWM), we also had access
to historical ABFT specimens collected by one of the authors
(M.S.) in the CWM tuna traps between 1911 and 1926 (Fig. S1).
Author contributions: M.L., G.B, and F.T. designed research; M.L., G.F., I.M., A.C., and M.S.
performed research; G.R.,M.L., G.F., and L.Z. analyzed data; and G.R., G.F., L.Z.,
G.B, and
F.T. wrote the paper.
The authors declareno conflict of inte
rest.
This article is a PNAS Direct Submission. B.B. is a guest editor inv
ited by the Editorial Board.
1G.R. and M.L. contributedequally to this work.
2Present address: Department of Biology,
University of Minho, Campus de Gualtar, 4710–
057 Braga, Portugal.
3Deceased April 9, 1959.
4To whom correspondenceshould be addressed at: Department of Experim
ental Evolu-
tionary Biology, University of Bologna, via
Selmi 3, 40126 Bologna, Italy.E-mail: fausto.
This article contains supporting information online at www.pnas.org/cgi/content/full/
0908281107/DCSupplemental.
2102–2107 | PNAS | February 2, 2010 | vol. 107 | no. 5
www.pnas.org/cgi/doi/10.1073/pnas.
0908281107
TECHNICAL NOTE
Isolation and characterization of microsatellite markers
for the heavily exploited rockfish Sebastes schlegeli,
and cross-species amplification in four related Sebastes spp.
Hye Suck An Æ Jung Youn Park Æ Mi-Jung Kim Æ
Eun Young Lee Æ Kyung Kil Kim
Received: 19 February 2009 / Accepted: 24 February 2009 / Published online: 7 March 2009
! Springer Science+Business Media B.V. 2009
Abstract Here we report development and characteriza-
tion of 14 polymorphic microsatellite loci from Sebastes
schlegel. Polymorphism at these loci revealed from 3 to 23
alleles. The observed heterozygosity ranged from 0.34 to
1.00, and the expected heterozygosity ranged from 0.31 to
0.95. No linkage disequibrium was found. Two loci were
significantly deviated from HWE (P\ 0.01). The 14 loci
were also surveyed in four other Sebastes species and 12
loci successfully amplified, where allelic diversity ranged
from highly polymorphic to monomorphic. These results
demonstrate these microsatellite markers can be used for
the study of intra- and inter-specific genetic diversity.
Keywords Sebastes schlegel ! Rockfish !
Microsatellites markers ! Cross-amplification
Introduction
Rockfish Sebastes schlegeli, belonging to the family
Sebastinae and an important commercial fish in Korea, is
one of the species for which artificial reproduction and
cultivation have intensively been made throughout Korean
coastal areas to increase the harvest yield since the early
1990s. A stock enhancement program through the release
of hatchery-raised juveniles into natural environments has
been practiced since the middle 1990s. In 2007, approxi-
mately two million seeds were released. In stock
enhancement programs, the genetic characterization of the
stocking species used should be assessed in view of
elucidating and monitoring the effect of such activities on
wild stocks (FAO 1993). Therefore, in recent years, the
extent of stocking impacts upon indigenous populations has
been a focus of attention from viewpoints of conservation
and management for this species. However, to date little is
known about genetic diversity and population differentia-
tion of this species. Information regarding population
structure, levels of geneflow and genetic diversity within
and among populations of species harvested for com-
mercial purposes can provide useful information for
developing conservation and management plans.
Although six microsatellite markers from S. schlegeli
have been already reported by Yoshida et al. (2005), a set
of molecular markers are needed for various other appli-
cations, from further population studies to pedigree
analysis. In this work, we isolated 14 novel microsatellite
markers from S. schlegeli, and represented their evaluation
for cross-species amplification in four other related con-
generic species.
We developed a partial genomic library enriched for CA
repeats as described in the protocol of Hamilton et al.
(1999) with a slight modification using prehybridization
PCR amplification (Gardner et al. 1999). Genomic DNA
was extracted from each fin tissue sample of S. schlegel
captured in western coast of Korea using TNES-Urea
buffer method (Asahida et al. 1996). DNA was simulta-
neously digested with restriction enzymes AluI, RsaI, NheI
and HhaI (New England Biolabs, Bervery, MA, USA).
DNA fragments ranging from 300 to 800 bp were isolated
and ligated to double-stranded linker-adapted primers
(SNX/SNX rev linker sequences). Linker-ligated DNA
fragments were then amplified using single-stranded linker-
adapted primer (SNX) as polymerase chain reaction
primer. Biotinylated dinucleotide repeat sequences [50-
(CA)12GCTTGA-biotin (Li et al. 2002)] were hyb
ridized toH. S. An (&) ! J. Y. Park ! M.-J. Kim ! E. Y. Lee ! K. K. Kim
Biotechnology Research Institute, National Fisheries Research
and Development Institute, Busan 619-705, Korea
e-mail: [email protected]
123
Conserv Genet (2009) 10:1969–1972
DOI 10.1007/s10592-009-9870-8
Demogr
aphic his
tory, g
eograp
hical d
istrib
ution
andrep
roduct
ive
isolat
ionof
distin
ctline
ages of
blue roc
kfish (Se
bastes
mystinu
s),
a marine
fishwith
a high dis
persal
potent
ial
M. O. B
URFO
RD
Departm
entof E
cology
andEvo
lutiona
ry Biolo
gy,Un
iversity
of Calif
ornia San
ta Cruz, S
anta Cru
z, CA,
USA
Introd
uction
Conte
mporary
andevo
lution
arytim
e-scal
e factor
s such
ascur
rent or
wind
patter
ns,geo
graphi
calbar
riers,
demogr
aphic
charac
teristi
cs,phy
sical cha
nges in
the
enviro
nment
, or a
combin
ation of
these
factor
s can
act
tored
ucegen
e flowam
ongpop
ulation
s throug
hout a
specie
s’ rang
e (Avise,
1994).
Inmarin
e system
s, redu
c-
tionor
elimina
tionin
gene flow
maylea
d togen
etic
differe
ntiatio
n orspe
ciation
even wit
hinspe
cies wit
h
long p
elagic
stages
, espec
ially if
popula
tions ar
e separ
ated
into diff
erent
ecolog
ical re
gions.
Select
ivefor
cescan
also
lead to
genetic
structu
reor
specia
tionin
marine tax
a
with a lon
g pelagi
c stage
only if i
t isstro
ngeno
ughto
counte
ract the
homoge
nizing
effect
ofgen
e flow. T
he
evalua
tionof t
hegen
eticrela
tionshi
p among
popula
tions
ordis
tinct
lineage
s inare
aswh
erediv
ergent
lineage
s
overlap
andwh
ereonl
y one
lineage
is foun
d can
improve
ourun
dersta
nding
of the
evolut
ionary
forces
andeve
nts
causin
gspe
ciation
inthe
marine
enviro
nment
. For
example
, high
potent
ialdis
persal
maynot
transl
ateto
high lev
elsof
realize
d gene flow
. We mayalso
gain
insigh
t into
why
there
ishig
hspe
cies div
ersity
in
taxono
mic grou
pswit
h high dis
persal
potent
ial.
Althou
ghthe
rockfis
hes(Sc
orpaen
idae:
Sebaste
s)are
consid
ered a
n ancien
t speci
es flock
(John
s &Av
ise,199
8)
with a hig
h potent
ialfor
disper
sal(th
rough
a pelagi
c
stage
lasting
2–5mont
hs;Lov
e et al.,
2002),
there
is
eviden
ceof
recent
specia
tionwit
hinthe
genus.
Rocha
-
Olivar
eset a
l. (199
9a)fou
ndrec
entspe
ciation
betwe
en
sister-
taxa in
thesub
genus
Sebasto
mus. T
woinv
estiga
-
tions wit
hinroc
kfish
specie
s found
cryptic
specia
tion
within
vermilio
n rockfis
h (Sebas
tesmin
iatus)
that wa
s
caused
bydiff
erence
indep
thdis
tributi
on(Hy
deet a
l.,
2008)
anda sim
ilarpat
tern of
sympat
ricdis
tributi
onof
distin
ctgen
eticpop
ulation
s ofPac
ificoce
anper
ch
Corresp
ondenc
e: Mart
haO.
Burfo
rd,208
Fernow
Hall, C
ornell
Unive
rsity,
Ithaca
, NY 148
53,US
A.
Tel.: +
1 831419
7586; f
ax:+1
831459
3383; e
-mail:
mob8@c
ornell.
edu
ª 2 009
THE AU
THOR . J
. EVO
L .B I O
L .2 2
( 2 00 9
) 14 7
1 –1 4
86
JOURNAL
COMP I LA T
I ON ª 2009
EUROPE
ANSO
C I E TY FO
R EVOLU
T IONAR
Y B IO LOGY
1471
Keywor
ds:
admixtu
re;
assign
menttes
t;
microsat
ellite loc
i;
mismatc
h distrib
ution;
mtDNA con
trol re
gion;
popula
tionexp
ansion
;
reprod
uctive
isolati
on;
specia
tion.
Abstr
act
Under
standi
ngthe
barrier
s togen
eticexc
hange
in taxono
mic grou
ps that
have
a high dis
persal
potent
ialwil
l prov
idecrit
ical in
formatio
n onspe
ciation
in
genera
l. Blue
rockfis
h (Sebas
tesmy
stinus)
aregoo
d taxa to
examine
specia
tion
becaus
e they are
nonmigra
tory inh
abitan
tsof
shallow
rocky
reef hab
itats
along
theeas
tern No
rthPac
ificwit
h a pela
giclarv
al stag
e lastin
g 3–5
months.
Thegoa
l ofthi
s study
was to
analyse
theevo
lution
aryhis
tory a
nddis
tributi
on
patter
nsof
differe
ntline
ages w
ithin
S. mysti
nusdes
cribed
previo
usly and
use
this in
formatio
n toun
dersta
ndthe
specia
tionpro
cess in
this g
roup of
high
disper
salfish
. Themole
cular
data der
ived fro
mspe
cimens
sample
d over
approx
imately
1650 km
ofthe
S.my
stinus
range
reveal
eda nor
therly
and
southe
rlydis
tributi
onfor
thetwo
lineage
s. Almost
equal f
requen
cies o
f both
lineage
s occurr
edat
centra
llyloc
ated sam
pleloc
ations,
with evi
dence
of
reprod
uctive
isolati
onbet
ween
theline
ages. A
demogr
aphic a
nalysis
showe
d
that th
e two line
ages d
iverge
d andexp
erience
d sudden
expans
ionpri
orto the
lastgla
cial maxi
mum, wh
ichaffe
cted
theobs
erved
patter
nof
genetic
structu
re.The
spatial
distrib
ution,
demogr
aphic h
istory
anddeg
reeof g
enetic
distin
ctivene
ss foun
d from
thegen
eticana
lysis, d
espite
thehig
h potent
ialfor
disper
salin
S. mysti
nus, su
ggest b
othline
ages d
iverge
d inallo
patry.
doi: 10
.1111/
j.1420-
9101.2
009.01
760.x
Mar BiolDOI 10.1007/s00227-010-1419-3
123
ORIGINAL PAPER
Life history, ecology and the biogeography of strong genetic breaks among 15 species of PaciWc rockWsh, SebastesArjun Sivasundar · Stephen R. Palumbi
Received: 15 April 2009 / Accepted: 2 March 2010© Springer-Verlag 2010
Abstract Strong genetic change over short spatial scalesis surprising among marine species with high dispersalpotential. Concordant breaks among several species signalsa role for geographic barriers to dispersal. Along the coastof California, such breaks have not been seen across thebiogeographic barrier of Point Conception, but other poten-tial geographic boundaries have been surveyed less often.We tested for strong-population structure in 11 species ofSebastes sampled across two regions containing potentialdispersal barriers, and conducted a meta-analysis includingfour additional species. We show two strong breaks northof Monterey Bay, spanning an oceanographic gradient andan upwelling jet. Moderate genetic structure is just as com-mon in the north as it is in the south, across the biogeo-graphic break at Point Conception. Gene Xow is generallyhigher among deep-water species, but these conclusions areconfounded by phylogeny. Species in the subgenus Sebast-osomus have higher structure than those in the subgenusPteropodus, despite having larvae with longer pelagicphases. DiVerences in settlement behavior in the face ofocean currents might help explain these diVerences. Acrosssimilar species across the same coastal environment, we
document a wide variety of patterns in gene Xow, suggest-ing that interaction of individual species traits such assettlement behavior with environmental factors such asoceanography can strongly impact population structure.
Introduction
For many marine species, larval dispersal is a critical partof migration ability, and life history diVerences betweenspecies can dramatically aVect gene Xow. Investigations ofgenetic diVerences among marine populations have beenwidely used to gauge levels of dispersal, which often scalewith larval traits such as pelagic duration (e.g. Berger 1973;Bohonak 1999; Marko 2004). Species for which larvalduration is short or absent have often been found to havestrong genetic structure among invertebrates (McMillanet al. 1992; Hellberg 1994, 1996) and Wshes (e.g. Waples1987; Doherty et al. 1995; Riginos 2001; Purcell et al.2006). However, unexpectedly strong structure has alsobeen demonstrated for some species that are presumed tohave long distance dispersal potential (e.g. Reeb et al.2000; Barber et al. 2002; Burford and Bernardi 2008).Uncovering the reasons for strong genetic breaks in suchspecies can potentially reveal a great deal about larvalmechanisms that limit dispersal.Some of the clearest explanations of strong geneticbreaks derive from the observation that in some cases, thesebreaks are concordant with strong biogeographic bound-aries. Taxa as diverse as coastal birds, tortoises, Wsh andinvertebrates show strong geographic diVerentiation alongthe southeastern coast of the United States (Avise 1992,1996). Other cases of the conXuence of genetic and biogeo-graphic breaks in the oceans have been found in Indonesia,the western Mediterranean, the East PaciWc and the Red Sea
Communicated by M. I. Taylor.A. Sivasundar · S. R. PalumbiDepartment of Biological Sciences, Hopkins Marine Station, Stanford University, 120 Oceanview Boulevard, PaciWc Grove, CA 93950, USA
A. Sivasundar (&)Division of Aquatic Ecology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012 Bern, Switzerlande-mail: [email protected]
National Oceanic and Atmospheric Administration
Data
• Microsatellite diversity – 202 studies of 140 species
– Number of alleles (A)
– Heterozygosity (He)
Available online at www.sciencedirect.com
Fisheries Research 89 (2008) 196–209
Stock identity of horse mackerel (Trachurus trachurus) in the Northeast
Atlantic and Mediterranean Sea: Integrating the results from
different stock identification approaches
P. Abaunza a,∗, A.G. Murta b, N. Campbell c, R. Cimmaruta d, A.S. Comesana e, G. Dahle f,
M.T. Garcıa Santamarıa g, L.S. Gordo h, S.A. Iversen f, K. MacKenzie c, A. Magoulas i,
S. Mattiucci j, J. Molloy k, G. Nascetti d, A.L. Pinto b, R. Quinta b, P. Ramos b,
A. Sanjuan e, A.T. Santos b, C. Stransky l, C. Zimmermann m
a Instituto Espanol de Oceanografıa, P.O. Box 240, 39080 Santander, Spain
b Instituto de Investigacao das Pescas e do Mar, Av. Brasilia, 1400 Lisboa, Portugal
c School of Biological Sciences (Zoology), The University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
d Department of Ecology and Sustainable Economic Development, Tuscia University, Via S. Giovanni Decollato, 1, 01100 Viterbo, Italy
e Facultade de Bioloxıa, Edificio de Ciencias, Universidade de Vigo, E-36200 Vigo, Spain
f Institute of Marine Research, P.O. Box 1870, Nordnes, N-5817 Bergen, Norway
g Instituto Espanol de Oceanografıa, Avda. Tres de Mayo 73, 38005 Santa Cruz de Tenerife, Spain
h Facultade de Ciencias de Lisboa (IO/DBA), Bloco C-2, Campo Grande, 1749-016 Lisboa, Portugal
i Hellenic Centre for Marine Research, Institute of Marine Biology and Genetics, P.O. Box 2214, GR 710 013 Iraklio, Greece
j Department of Public Health Sciences, Section of Parasitology, “Sapienza” University of Rome, piazzale Aldo Moro n◦ 5, 00185 Rome, Italy
k The Marine Institute, Parkmore Industrial Estate, Galway, Ireland
l Bundesforschungsanstalt fur Fischerei, Institut fur Seefischerei, Palmaille 9, D-22767 Hamburg, Germany
m Bundesforschungsanstalt fur Fischerei, Institut fur Ostseefischerei, Alter Hafen Su 2, D-18069 Rostock, Germany
AbstractHorse mackerel stock identification was carried out with the aim of obtaining management units that were meaningful biological entities and
thus improving the management of the resource. The stock identification was made by integrating both established and innovative approaches such
as genetic markers (allozymes, mitochondrial DNA, microsatellite DNA and SSCP on nuclear DNA), morphometry, parasites as biological tags,
and life history traits (growth, reproduction and distribution), within the EU-funded HOMSIR project. The sampling covered almost the whole
distribution range of horse mackerel through 20 sampling localities in Northeast Atlantic and Mediterranean Sea. Horse mackerel showed low
levels of genetic differentiation, stable genetic structure over the study time and high levels of genetic variability. However, several approaches
(morphometrics and parasites) support the separation between the Atlantic Ocean and the Mediterranean Sea in horse mackerel populations,
although the most western Mediterranean area could also be mixed with the Atlantic populations. In the Northeast Atlantic, various stocks can be
distinguished mainly based on morphometrics, parasites and life history traits: a “southern” stock is distributed along the West Atlantic coast of
the Iberian Peninsula south to Cape Finisterre (NW Spain); a “western” stock, along the west coast of Europe from Cape Finisterre to Norway and
the “North Sea” stock. These results implied the revision of the boundaries of the southern and western stocks as previously defined. Results also
suggested that adult horse mackerel could migrate through different areas following the west coasts in the Northeast Atlantic (i.e. between Celtic
Seas and northern North Sea). Horse mackerel from the Mauritanian coast is distinguished by its high growth rate and high batch fecundity. Based
on the results from morphometric analysis and the use of parasites as biological tags, the horse mackerel population in the Mediterranean Sea is
sub-structured into at least three main areas: western, central and eastern Mediterranean. In this contribution, we have integrated the fundamental
findings of different approaches showing that the holistic approach is the appropriate way to identify horse mackerel stocks, on covering multiple
aspects of the biology of the species and reducing the type I error in stock identification.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Trachurus trachurus; Stock identity; Holistic approach; Northeast Atlantic; Mediterranean Sea; Natural marks; Life history traits
∗ Corresponding author. Tel.: +34 942291060; fax: +34 942275072.
E-mail address: [email protected] (P. Abaunza).
0165-7836/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.fishres.2007.09.022
Spatio-temporal populationstructuring and genetic
diversity retention in depleted Atlantic Bluefin tuna
of the Mediterranean Sea
Giulia Riccionia,1, Monica Landi
b,1,2, Giorgia Ferrarab, Ilaria Milano
b, Alessia Carianib, Lorenzo Zane
c, Massimo Sellad,3,
Guido Barbujania, and Fausto Tinti
b,4
aDepartment of Biologyand Evolution, Univ
ersity of Ferrara, 44100 Ferrara, Italy;
bDepartment of Experimental Evolution
ary Biology, University of Bologna,
40126 Bologna, Italy;cDepartment of Biology,
University of Padova, 35121 Padova, Italy; a
nd dInstitute Center for Marine Research, 52210 Rovinj, Croatia
(formerly Istituto Italo-Germanico di Biologia Marina/Deutsch-Italienisches Ins
titut für Meersbiologie, Rovigno, Italy)
Edited by Barbara Block, StanfordUniversity, Stan
ford, CA, and accepted by the Editorial BoardDecember 1, 2009 (received for review July 24, 2009)
Fishery genetics have greatly changed our understandingof
population dynamics and structuring in marine fish. In this study,
we show that theAtlantic Bluefin tuna (ABFT, Thu
nnus thynnus),an
oceanic predatory species exhibiting highly migratory behavior,
large population size, and high potential for dispersal during
early
life stages, displays significant ge
netic differences over space and
time, both at the fine and large scales of variation. We compared
microsatellite variationof contem
porary (n=256) andhistorical (n=
99) biological samples of ABFTs of the central-western Mediterra-
nean Sea, the latter dating back to the early 20th century.Measures
of genetic differentiationand a general hetero
zygote deficit sug-
gest that differences exist among population samples, both now
and 96–80 years ago. Thus, ABFTs do not represent a
single panmic-
tic population in theMediterranean Sea. Statistics designed to infer
changes in population size, both from current and past genetic var-
iation, suggest that some Mediterranean ABFT populations,
although still not severely reduced in their genetic po
tential, might
have suffered fromdemographic declines. The short-te
rmestimates
of effectivepopulation sizeare straddle
don theminimumthreshold
(effectivepopulationsize=500) indicatedt
omaintaingeneticdiver-
sity and evolutionary potential across several generations in
natural populations.
ancient DNA | effective population size | genetic structure | large pelagic
fishes | Thunnus thynnus
With an impressive amount of data accumulated in the last
10–15 years, genetic studies have greatly changed our
understanding of the ecology and evolution of marine fish pop-
ulations by showing evidence of complex genetic struc
ture at the
spatial and temporal scales of variation. This is esp
ecially true for
fish species with high mobility, high potential for dispersal during
egg and larval stages, andlarge population sizes (1, 2). Accurate
estimates of genetic variation in fish populations, both
for neutral
and adaptive loci, can also suggest unique strategies for stock
management and conservation of evolutionary potential in
severely exploited fishery resources (3–5). The assessment of
population dynamics, environmentally driven changes, and levels
of exploitation in large pelagic fish is crucial for bothstock man-
agement and conservation of marine ecosystems dominated by
these oceanic toppredators (6). Although fisheries s
till remain the
chief source of data for assessing spatiotemporal population
dynamics of these fish (7–10), wheneverpossible, their findings
shouldbe comparedwith thoseoffishery-independ
ent approaches,
such as genetic, electronic, andmicrochemical tagging experi
ments
(11–13), to have more accurate data on the key features of pop-
ulation dynamics, such as spawning and migrations (10).
The Atlantic Bluefin tuna (ABFT, Thunnus thynnus) is a large
top-predator fishexploiting the pelagic ecosystems of the North
Atlantic Ocean andMediterranean Sea.Much like the other
large
tunas, the ABFT displays highly migratory behavior, with docu-
mented transoceanic andlarge-scale movements for feeding and
reproduction, high fecundity, and high mortality of larval stages
(reviewed in 14, 15). Nonetheless, tagging experiments and fish-
ery data analyses have unraveled an unexpected and complex
interplay of ecological, behavioral,
and reproductive factors that
could affect the spatial and temporal populationdynamics at the
large scale (11, 16). Microchemical signatures in otoliths of
yearlings (i.e., young-of-the-year) unequivocally identified two
main spawning areas [i.e., the Mediterranean Sea for the Easte
rn
Atlantic population, the Gulf of Mexico for the Western Atlantic
population (13)]. Because of high rates of natal homing of
spawning adults to their native areas (95.8% for the Medi-
terranean Sea and 99.3% for the Gulf of Mexico) and limited and
more complex movements in sexually mature ABFTs (11, 17), the
two populations show significant genetic divergence at both
microsatellite (12) and mtDNA (18) loci. The two ABFT pop-
ulations differ insize, with the eastern population approximately
10 times as large as the western population (19). Both are suf-
fering from overfishing and are considered depleted, consistent
with the continuous decline of the spawning stock biomass
(which, in the eastern stock, is now at 40% of the 1970s levels),
with the high fishing mortality rate of age class 8 and older indi-
viduals, and with modeling predictions (16, 19, 20).
The complex population dynamics exhibited by ABFTs at the
large scale is also apparent at a finer scale in the Mediterranean
Sea (16). Size-dependent movements and spawning in different
areas and periods have been documented (15, 21–23). Genetic
variation among three geographical samples suggested that at
least two subpopulations inhabit and persist over short time
periods (3 years) in the western and eastern Mediterranean Sea,
yielding Wright’s genetic variance (FST) values within the Med-
iterranean Sea between 0.0007 and 0.0087 (12, 24). In this study,
we started from a more thorough sampling of Mediterranean
ABFTs in space and time. Along with an extensive spatial sam-
pling of contemporary ABFTs carried out from 1999 to 2007 in
the central-western Mediterranean (CWM), we also had access
to historical ABFT specimens collected by one of the authors
(M.S.) in the CWM tuna traps between 1911 and 1926 (Fig. S1).
Author contributions: M.L., G.B, and F.T. designed research; M.L., G.F., I.M., A.C., and M.S.
performed research; G.R.,M.L., G.F., and L.Z. analyzed data; and G.R., G.F., L.Z.,
G.B, and
F.T. wrote the paper.
The authors declareno conflict of inte
rest.
This article is a PNAS Direct Submission. B.B. is a guest editor inv
ited by the Editorial Board.
1G.R. and M.L. contributedequally to this work.
2Present address: Department of Biology,
University of Minho, Campus de Gualtar, 4710–
057 Braga, Portugal.
3Deceased April 9, 1959.
4To whom correspondenceshould be addressed at: Department of Experim
ental Evolu-
tionary Biology, University of Bologna, via
Selmi 3, 40126 Bologna, Italy.E-mail: fausto.
This article contains supporting information online at www.pnas.org/cgi/content/full/
0908281107/DCSupplemental.
2102–2107 | PNAS | February 2, 2010 | vol. 107 | no. 5
www.pnas.org/cgi/doi/10.1073/pnas.
0908281107
TECHNICAL NOTE
Isolation and characterization of microsatellite markers
for the heavily exploited rockfish Sebastes schlegeli,
and cross-species amplification in four related Sebastes spp.
Hye Suck An Æ Jung Youn Park Æ Mi-Jung Kim Æ
Eun Young Lee Æ Kyung Kil Kim
Received: 19 February 2009 / Accepted: 24 February 2009 / Published online: 7 March 2009
! Springer Science+Business Media B.V. 2009
Abstract Here we report development and characteriza-
tion of 14 polymorphic microsatellite loci from Sebastes
schlegel. Polymorphism at these loci revealed from 3 to 23
alleles. The observed heterozygosity ranged from 0.34 to
1.00, and the expected heterozygosity ranged from 0.31 to
0.95. No linkage disequibrium was found. Two loci were
significantly deviated from HWE (P\ 0.01). The 14 loci
were also surveyed in four other Sebastes species and 12
loci successfully amplified, where allelic diversity ranged
from highly polymorphic to monomorphic. These results
demonstrate these microsatellite markers can be used for
the study of intra- and inter-specific genetic diversity.
Keywords Sebastes schlegel ! Rockfish !
Microsatellites markers ! Cross-amplification
Introduction
Rockfish Sebastes schlegeli, belonging to the family
Sebastinae and an important commercial fish in Korea, is
one of the species for which artificial reproduction and
cultivation have intensively been made throughout Korean
coastal areas to increase the harvest yield since the early
1990s. A stock enhancement program through the release
of hatchery-raised juveniles into natural environments has
been practiced since the middle 1990s. In 2007, approxi-
mately two million seeds were released. In stock
enhancement programs, the genetic characterization of the
stocking species used should be assessed in view of
elucidating and monitoring the effect of such activities on
wild stocks (FAO 1993). Therefore, in recent years, the
extent of stocking impacts upon indigenous populations has
been a focus of attention from viewpoints of conservation
and management for this species. However, to date little is
known about genetic diversity and population differentia-
tion of this species. Information regarding population
structure, levels of geneflow and genetic diversity within
and among populations of species harvested for com-
mercial purposes can provide useful information for
developing conservation and management plans.
Although six microsatellite markers from S. schlegeli
have been already reported by Yoshida et al. (2005), a set
of molecular markers are needed for various other appli-
cations, from further population studies to pedigree
analysis. In this work, we isolated 14 novel microsatellite
markers from S. schlegeli, and represented their evaluation
for cross-species amplification in four other related con-
generic species.
We developed a partial genomic library enriched for CA
repeats as described in the protocol of Hamilton et al.
(1999) with a slight modification using prehybridization
PCR amplification (Gardner et al. 1999). Genomic DNA
was extracted from each fin tissue sample of S. schlegel
captured in western coast of Korea using TNES-Urea
buffer method (Asahida et al. 1996). DNA was simulta-
neously digested with restriction enzymes AluI, RsaI, NheI
and HhaI (New England Biolabs, Bervery, MA, USA).
DNA fragments ranging from 300 to 800 bp were isolated
and ligated to double-stranded linker-adapted primers
(SNX/SNX rev linker sequences). Linker-ligated DNA
fragments were then amplified using single-stranded linker-
adapted primer (SNX) as polymerase chain reaction
primer. Biotinylated dinucleotide repeat sequences [50-
(CA)12GCTTGA-biotin (Li et al. 2002)] were hyb
ridized toH. S. An (&) ! J. Y. Park ! M.-J. Kim ! E. Y. Lee ! K. K. Kim
Biotechnology Research Institute, National Fisheries Research
and Development Institute, Busan 619-705, Korea
e-mail: [email protected]
123
Conserv Genet (2009) 10:1969–1972
DOI 10.1007/s10592-009-9870-8
Demogr
aphic his
tory, g
eograp
hical d
istrib
ution
andrep
roduct
ive
isolat
ionof
distin
ctline
ages of
blue roc
kfish (Se
bastes
mystinu
s),
a marine
fishwith
a high dis
persal
potent
ial
M. O. B
URFO
RD
Departm
entof E
cology
andEvo
lutiona
ry Biolo
gy,Un
iversity
of Calif
ornia San
ta Cruz, S
anta Cru
z, CA,
USA
Introd
uction
Conte
mporary
andevo
lution
arytim
e-scal
e factor
s such
ascur
rent or
wind
patter
ns,geo
graphi
calbar
riers,
demogr
aphic
charac
teristi
cs,phy
sical cha
nges in
the
enviro
nment
, or a
combin
ation of
these
factor
s can
act
tored
ucegen
e flowam
ongpop
ulation
s throug
hout a
specie
s’ rang
e (Avise,
1994).
Inmarin
e system
s, redu
c-
tionor
elimina
tionin
gene flow
maylea
d togen
etic
differe
ntiatio
n orspe
ciation
even wit
hinspe
cies wit
h
long p
elagic
stages
, espec
ially if
popula
tions ar
e separ
ated
into diff
erent
ecolog
ical re
gions.
Select
ivefor
cescan
also
lead to
genetic
structu
reor
specia
tionin
marine tax
a
with a lon
g pelagi
c stage
only if i
t isstro
ngeno
ughto
counte
ract the
homoge
nizing
effect
ofgen
e flow. T
he
evalua
tionof t
hegen
eticrela
tionshi
p among
popula
tions
ordis
tinct
lineage
s inare
aswh
erediv
ergent
lineage
s
overlap
andwh
ereonl
y one
lineage
is foun
d can
improve
ourun
dersta
nding
of the
evolut
ionary
forces
andeve
nts
causin
gspe
ciation
inthe
marine
enviro
nment
. For
example
, high
potent
ialdis
persal
maynot
transl
ateto
high lev
elsof
realize
d gene flow
. We mayalso
gain
insigh
t into
why
there
ishig
hspe
cies div
ersity
in
taxono
mic grou
pswit
h high dis
persal
potent
ial.
Althou
ghthe
rockfis
hes(Sc
orpaen
idae:
Sebaste
s)are
consid
ered a
n ancien
t speci
es flock
(John
s &Av
ise,199
8)
with a hig
h potent
ialfor
disper
sal(th
rough
a pelagi
c
stage
lasting
2–5mont
hs;Lov
e et al.,
2002),
there
is
eviden
ceof
recent
specia
tionwit
hinthe
genus.
Rocha
-
Olivar
eset a
l. (199
9a)fou
ndrec
entspe
ciation
betwe
en
sister-
taxa in
thesub
genus
Sebasto
mus. T
woinv
estiga
-
tions wit
hinroc
kfish
specie
s found
cryptic
specia
tion
within
vermilio
n rockfis
h (Sebas
tesmin
iatus)
that wa
s
caused
bydiff
erence
indep
thdis
tributi
on(Hy
deet a
l.,
2008)
anda sim
ilarpat
tern of
sympat
ricdis
tributi
onof
distin
ctgen
eticpop
ulation
s ofPac
ificoce
anper
ch
Corresp
ondenc
e: Mart
haO.
Burfo
rd,208
Fernow
Hall, C
ornell
Unive
rsity,
Ithaca
, NY 148
53,US
A.
Tel.: +
1 831419
7586; f
ax:+1
831459
3383; e
-mail:
mob8@c
ornell.
edu
ª 2 009
THE AU
THOR . J
. EVO
L .B I O
L .2 2
( 2 00 9
) 14 7
1 –1 4
86
JOURNAL
COMP I LA T
I ON ª 2009
EUROPE
ANSO
C I E TY FO
R EVOLU
T IONAR
Y B IO LOGY
1471
Keywor
ds:
admixtu
re;
assign
menttes
t;
microsat
ellite loc
i;
mismatc
h distrib
ution;
mtDNA con
trol re
gion;
popula
tionexp
ansion
;
reprod
uctive
isolati
on;
specia
tion.
Abstr
act
Under
standi
ngthe
barrier
s togen
eticexc
hange
in taxono
mic grou
ps that
have
a high dis
persal
potent
ialwil
l prov
idecrit
ical in
formatio
n onspe
ciation
in
genera
l. Blue
rockfis
h (Sebas
tesmy
stinus)
aregoo
d taxa to
examine
specia
tion
becaus
e they are
nonmigra
tory inh
abitan
tsof
shallow
rocky
reef hab
itats
along
theeas
tern No
rthPac
ificwit
h a pela
giclarv
al stag
e lastin
g 3–5
months.
Thegoa
l ofthi
s study
was to
analyse
theevo
lution
aryhis
tory a
nddis
tributi
on
patter
nsof
differe
ntline
ages w
ithin
S. mysti
nusdes
cribed
previo
usly and
use
this in
formatio
n toun
dersta
ndthe
specia
tionpro
cess in
this g
roup of
high
disper
salfish
. Themole
cular
data der
ived fro
mspe
cimens
sample
d over
approx
imately
1650 km
ofthe
S.my
stinus
range
reveal
eda nor
therly
and
southe
rlydis
tributi
onfor
thetwo
lineage
s. Almost
equal f
requen
cies o
f both
lineage
s occurr
edat
centra
llyloc
ated sam
pleloc
ations,
with evi
dence
of
reprod
uctive
isolati
onbet
ween
theline
ages. A
demogr
aphic a
nalysis
showe
d
that th
e two line
ages d
iverge
d andexp
erience
d sudden
expans
ionpri
orto the
lastgla
cial maxi
mum, wh
ichaffe
cted
theobs
erved
patter
nof
genetic
structu
re.The
spatial
distrib
ution,
demogr
aphic h
istory
anddeg
reeof g
enetic
distin
ctivene
ss foun
d from
thegen
eticana
lysis, d
espite
thehig
h potent
ialfor
disper
salin
S. mysti
nus, su
ggest b
othline
ages d
iverge
d inallo
patry.
doi: 10
.1111/
j.1420-
9101.2
009.01
760.x
Mar BiolDOI 10.1007/s00227-010-1419-3
123
ORIGINAL PAPER
Life history, ecology and the biogeography of strong genetic breaks among 15 species of PaciWc rockWsh, SebastesArjun Sivasundar · Stephen R. Palumbi
Received: 15 April 2009 / Accepted: 2 March 2010© Springer-Verlag 2010
Abstract Strong genetic change over short spatial scalesis surprising among marine species with high dispersalpotential. Concordant breaks among several species signalsa role for geographic barriers to dispersal. Along the coastof California, such breaks have not been seen across thebiogeographic barrier of Point Conception, but other poten-tial geographic boundaries have been surveyed less often.We tested for strong-population structure in 11 species ofSebastes sampled across two regions containing potentialdispersal barriers, and conducted a meta-analysis includingfour additional species. We show two strong breaks northof Monterey Bay, spanning an oceanographic gradient andan upwelling jet. Moderate genetic structure is just as com-mon in the north as it is in the south, across the biogeo-graphic break at Point Conception. Gene Xow is generallyhigher among deep-water species, but these conclusions areconfounded by phylogeny. Species in the subgenus Sebast-osomus have higher structure than those in the subgenusPteropodus, despite having larvae with longer pelagicphases. DiVerences in settlement behavior in the face ofocean currents might help explain these diVerences. Acrosssimilar species across the same coastal environment, we
document a wide variety of patterns in gene Xow, suggest-ing that interaction of individual species traits such assettlement behavior with environmental factors such asoceanography can strongly impact population structure.
Introduction
For many marine species, larval dispersal is a critical partof migration ability, and life history diVerences betweenspecies can dramatically aVect gene Xow. Investigations ofgenetic diVerences among marine populations have beenwidely used to gauge levels of dispersal, which often scalewith larval traits such as pelagic duration (e.g. Berger 1973;Bohonak 1999; Marko 2004). Species for which larvalduration is short or absent have often been found to havestrong genetic structure among invertebrates (McMillanet al. 1992; Hellberg 1994, 1996) and Wshes (e.g. Waples1987; Doherty et al. 1995; Riginos 2001; Purcell et al.2006). However, unexpectedly strong structure has alsobeen demonstrated for some species that are presumed tohave long distance dispersal potential (e.g. Reeb et al.2000; Barber et al. 2002; Burford and Bernardi 2008).Uncovering the reasons for strong genetic breaks in suchspecies can potentially reveal a great deal about larvalmechanisms that limit dispersal.Some of the clearest explanations of strong geneticbreaks derive from the observation that in some cases, thesebreaks are concordant with strong biogeographic bound-aries. Taxa as diverse as coastal birds, tortoises, Wsh andinvertebrates show strong geographic diVerentiation alongthe southeastern coast of the United States (Avise 1992,1996). Other cases of the conXuence of genetic and biogeo-graphic breaks in the oceans have been found in Indonesia,the western Mediterranean, the East PaciWc and the Red Sea
Communicated by M. I. Taylor.A. Sivasundar · S. R. PalumbiDepartment of Biological Sciences, Hopkins Marine Station, Stanford University, 120 Oceanview Boulevard, PaciWc Grove, CA 93950, USA
A. Sivasundar (&)Division of Aquatic Ecology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012 Bern, Switzerlande-mail: [email protected]
National Oceanic and Atmospheric Administration
Paired comparisons
Overfished populations
Healthy species and population in same genus or family
Pinsky et al. 2014 Molecular Ecology
Paired comparisons
Overfished populations
Healthy species and population in same genus or family
Pinsky et al. 2014 Molecular Ecology
Paired comparisons
Pinsky et al. 2014 Molecular Ecology
Other Pagrus
New Zealand snapper (Pagrus auratus)
A = 16 He = 0.7 A = 12 He = 0.8
Paired comparisons overfished vs. control
n = 12
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
A50 = 10.2He = 0.736
A50 = 16.6He = 0.846
Pinsky et al. Molecular Ecology
% More Alleles in Overfished
●
●
●
●
●
●
●
●
●
●
●
●
Osmeridae
Trachurus
Lutjanus
Serranidae
Sebastes
Gadidae
Scophthalmidae
Clupeidae
Pagrus
Pleuronectidae
Scombridae
Cynoscion
−50 −25 0 25 50
% difference in allelic richness
Drum
Tunas
Flounders
Seabream
Herrings
Turbots
Cods
Rockfishes
Groupers
Snappers
Jack mackerels
Smelts
% More Alleles in Overfished
●
●
●
●
●
●
●
●
●
●
●
●
Osmeridae
Trachurus
Lutjanus
Serranidae
Sebastes
Gadidae
Scophthalmidae
Clupeidae
Pagrus
Pleuronectidae
Scombridae
Cynoscion
−50 −25 0 25 50
Drum
Tunas
Flounders
Seabream
Herrings
Turbots
Cods
Rockfishes
Groupers
Snappers
Jack mackerels
Smelts
Pinsky et al. Molecular Ecology
% difference in allelic richness
% More Alleles in Overfished
●
●
●
●
●
●
●
●
●
●
●
●
Osmeridae
Trachurus
Lutjanus
Serranidae
Sebastes
Gadidae
Scophthalmidae
Clupeidae
Pagrus
Pleuronectidae
Scombridae
Cynoscion
−50 −25 0 25 50
Drum
Tunas
Flounders
Seabream
Herrings
Turbots
Cods
Rockfishes
Groupers
Snappers
Jack mackerels
Smelts
Pinsky et al. Molecular Ecology
% difference in allelic richness
% More Alleles in Overfished
●
●
●
●
●
●
●
●
●
●
●
●
Osmeridae
Trachurus
Lutjanus
Serranidae
Sebastes
Gadidae
Scophthalmidae
Clupeidae
Pagrus
Pleuronectidae
Scombridae
Cynoscion
−50 −25 0 25 50
Drum
Tunas
Flounders
Seabream
Herrings
Turbots
Cods
Rockfishes
Groupers
Snappers
Jack mackerels
Smelts
Pinsky et al. Molecular Ecology
Overfished populations have higher
diversity
Overfished populations have lower
diversity
% difference in allelic richness
% More Alleles in Overfished
●
●
●
●
●
●
●
●
●
●
●
●
Osmeridae
Trachurus
Lutjanus
Serranidae
Sebastes
Gadidae
Scophthalmidae
Clupeidae
Pagrus
Pleuronectidae
Scombridae
Cynoscion
−50 −25 0 25 50
Drum
Tunas
Flounders
Seabream
Herrings
Turbots
Cods
Rockfishes
Groupers
Snappers
Jack mackerels
Smelts
Pinsky et al. Molecular Ecology
% difference in allelic richness
% More Alleles in Overfished
●
●
●
●
●
●
●
●
●
●
●
●
Osmeridae
Trachurus
Lutjanus
Serranidae
Sebastes
Gadidae
Scophthalmidae
Clupeidae
Pagrus
Pleuronectidae
Scombridae
Cynoscion
−50 −25 0 25 50
Drum
Tunas
Flounders
Seabream
Herrings
Turbots
Cods
Rockfishes
Groupers
Snappers
Jack mackerels
Smelts
Pinsky et al. Molecular Ecology
9 of 12 groups have lower diversity in overfished populations
% difference in allelic richness
% More Alleles in Overfished
●
●
●
●
●
●
●
●
●
●
●
●
Osmeridae
Trachurus
Lutjanus
Serranidae
Sebastes
Gadidae
Scophthalmidae
Clupeidae
Pagrus
Pleuronectidae
Scombridae
Cynoscion
−50 −25 0 25 50
Drum
Tunas
Flounders
Seabream
Herrings
Turbots
Cods
Rockfishes
Groupers
Snappers
Jack mackerels
Smelts
Pinsky et al. Molecular Ecology
Average: 12% lower
% difference in allelic richness
Findings
• Weak bottleneck now
Findings
• Weak bottleneck now • Impacts likely started ~1950s: rapid!
Findings
• Weak bottleneck now • Impacts likely started ~1950s: rapid! • Becoming stronger with time
Findings
• Weak bottleneck now • Impacts likely started ~1950s: rapid! • Becoming stronger with time • Lower ability to adapt in the future
Summary
• Genetic diversity provides the raw material for evolution
Summary
• Genetic diversity provides the raw material for evolution
• Evolution is happening all around us
Summary
• Genetic diversity provides the raw material for evolution
• Evolution is happening all around us • Humans can influence the course of
evolution
Top Related