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

33% blue 67% red

• Fitness: ability to pass genes on to future generations 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 Review Trends in Ecology and Evolution Vol.23 No.6 down to thousands might have no effect on heterozygosity, Box 2. Effects of trophy hunting but could result in a decline in allelic diversity [22]. By contrast, greater harvest of males through hunting in Trophy hunting (and fishing) targets individuals with certain ungulates could have limited effect on allelic diversity desirable phenotypes [66]. The result is increased mortality and reduced fitness of those individuals with desirable phenotypes. while reducing heterozygosity because NC (e.g. female Consequently, phenotypes that are considered desirable will numbers) can remain large even when Ne is reduced owing decrease in frequency. For example, populations of bighorn sheep to increasingly skewed sex ratios favoring females [33]. Ovis canadensis are often managed to provide a source of large- The loss of genetic variation will also be influenced by horned rams for trophy hunting [67]. In one population of bighorn sheep at Ram Mountain, Alberta, Canada, a total of 57 rams were gene flow among subpopulations that comprise a metapo- harvested under such an unrestricted management regime over a pulation. Estimating the effective population size of a 30 year period [67]. This corresponded to an average harvest rate of metapopulation is extremely complex [34]. In addition, 40% of the legal-sized rams in a given year, with the average age of  harvesting might have unexpected effects on the overall a ram at harvest of 6 years. Because rams in this population do not N of a metapopulation. For example, Hindar and col- generally reach their peak reproductive years until 8 years of age e [67], hunters imposed an artificial selection pressure on horn size leagues have found that small subpopulations within a that had the potential to bring about genetic change, provided that metapopulation of Atlantic salmon Salmo salar contribute the horn size was heritable. more per spawner to the overall effective population size The heritability of horn size, or any other quantitative trait, can be than large subpopulations, and harvesting of the subpopu- estimated using pedigree information [60]. Mother–offspring rela- lations jointly in mixed-stock fisheries has a relatively tionships in the Ram Mountain population were known through observation, and father–offspring relationships were determined larger demographic effect on small than large populations using microsatellites for paternity and sibship analyses [67]. An [35]. ‘animal model’ analysis (named as such because it estimates the expected genetic ‘breeding value’ [twice the expected deviation of Exploitative selection an individual’s offspring from the term population mean for the trait Selective genetic changes within subpopulations resulting being considered] for each individual animal in the population) was conducted, which uses relatedness across the entire pedigree to from exploitation are inevitable because increasing estimate narrow-sense heritability. Horn length was found to be mortality will result in selection for earlier maturation highly heritable (HN = 0.69) [67]. even if harvest is independent of phenotype [5]. Moreover, The examination of individual breeding values revealed that rams harvesting of wild populations is inevitably phenotypically with the highest breeding values were harvested earliest (Figure Ia) and therefore had lower fitness than rams of lower breeding value nonrandom [5]. That is, individuals of certain phenotypes [67]. As a consequence, the average horn length observed in the (e.g. sizes or behaviors) are more likely than others to be population has steadily declined (Figure Ib). Unrestricted harvesting removed from a wild population by harvesting. Such se- has therefore resulted in a decline inBighorn the trait that determines sheep trophy lective harvest will bring about genetic changes in har- quality (i.e. horn length) by removing desirable rams of high genetic vested populations if the favored phenotype has at least a quality before their reproductive peak. partial genetic basis (i.e. is heritable). In addition, such changes are likely to reduce both the frequency of desirable phenotypes (Box 2) and productivity. We use the term ‘exploitative selection’ for the process of selection 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 and plants. Rapid genetic change in response to strong selec- tion has been called ‘contemporary evolution’ [36]. How- ever, this term can be misleading because evolution is more than just change by natural selection. Thus, loss of genetic variation caused by genetic drift or increase in genetic variation caused by hybridization would also represent Figure I. (a) Breeding value (twice the expected deviation of an individual’s contemporary evolution. offspring from the term population mean) for horn length of trophy-harvested The rate of genetic change by exploitative selection male bighorn sheep at Ram Mountain. Males with greater breeding value are depends upon the amount of additive genetic variation harvested at a younger age and thus tend to haveColtman lower fitness et al. than 2003 males Nature with lower breeding value [67]. (b) Plot of mean ( SE) horn length of 4-year-old Æ for the trait (heritability): rams over a 30 year period showing the decline of mean horn length in this population. R H S; [1] ¼ N where HN is the narrow-sense heritability, S is the selection differential (the difference in the phenotypic There are many examples in the literature of phenotypic means between the selected parents and the whole popu- changes in exploited populations that might be the result of lation) and R is the response (the difference in the exploitative selection (Table 2). However, it has been diffi- phenotypic means between the progeny generation and cult to determine whether observed phenotypic changes the whole population in the previous generation) [32].In over time indicate genetic change or are caused by other the case of exploitative selection, S will be affected both factors such as relaxing density-dependent effects on by the intensity of harvest (the proportion of the indi- growth due to reductions in population density, or abiotic viduals harvested) and the phenotypic selectivity of the factors such as temperature affecting growth and devel- harvest. opment [37]. A recent review in this journal critically

331 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 Alleles: 2 Heterozygosity: 60% Heterozygosity: 40% Bottleneck examples

Robert Schwemmer Northern elephant seal

Florida panther Can fisheries cause bottlenecks?

Purse seiner for salmon Tuna, billfishes, swordfish Myers & Worm 2003 Nature Can fisheries cause bottlenecks?

Collapsed populations still abundant! Number of alleles (Ā) 10 11 12 A few examples? 7 8 9 1940 19601980 2000 New snapper ( Zealand Peter Halasz after Hauser

et al . 2002 Pagrus PNAS

auratus ) Number of alleles (Ā) 10 11 12 A few examples? 7 8 9 1940 19601980 2000 New snapper ( Zealand Peter Halasz after Hauser

et al . 2002 Pagrus PNAS

auratus ) Also: Also: – –

plaice plaice cod European Atlantic Number of alleles (Ā) 10 11 12 A few examples? 7 8 9 1940 19601980 2000 New snapper ( Zealand Peter Halasz after Hauser

et al . 2002 Pagrus PNAS

auratus ) But not: Also: – – – – – rockfish tuna cod plaice cod Canary Bluefin Atlantic European Atlantic

Data doi: 10.1111/j.1420-9101.2009.01760.x ),

Sebastes mystinus • Microsatellite diversity

Demographic history, geographical distribution and reproductive isolation of distinct lineages of blue rockfish ( – 202 studies of 140 species a marine fish with a high dispersal potential ) are good taxa to examine speciation

M. O. BURFORD Sebastes mystinus described previously and use Department of Ecology and Evolutionary Biology, University of CaliforniaAbstract Santa Cruz, Santa Cruz, CA, USA Understanding the barriers to genetic exchangeS. in mystinus taxonomic groups that have a high dispersal potential will provide critical information on speciation in range revealed a northerly and general. Blue rockfish ( because they are nonmigratory inhabitants of shallow rocky reef habitats S. mystinus along the eastern North Pacific with a pelagic larval stage lasting 3–5 months. Keywords: Available online at www.sciencedirect.comThe goal of this study was to analyse the evolutionary history and distribution patterns of different lineages within admixture; this information to understand the speciation process in this group of high assignment test; dispersal fish. The molecular data derived from specimens sampled over microsatellite loci; approximately 1650 km of the mismatch distribution;Fisheries Research 89 (2008) 196–209 southerly distribution for the two lineages. Almost equal frequencies of both Stock identity of horsemtDNA mackerelcontrol region; ( lineages occurred at centrally located sample locations, with evidence of population expansion; reproductive isolation between the lineages. A demographic analysis showed reproductive isolation; Atlantic and Mediterranean Sea: Integrating thethat results the two fromlineages diverged, suggest and experienced both lineages sudden diverged expansion in allopatry. prior to the speciation. last glacial maximum, which affected the observed pattern of genetic structure. The spatialS. mystinus distribution, demographic history and degree of genetic Trachurus trachurusdistinctiveness found from the genetic analysis, despite the high potential for P. Abaunza different stock identification approachesdispersal in a , ) are M.T. Garc ∗, A.G. Murta ) in the Northeastor distinct lineages in areas where divergent lineages ´ıa Santamar b Sebastes S. Mattiucci , N. Campbell overlap and where only one lineage is found can improve ´ıa g our understanding of the evolutionary forces and events j , L.S. Gordo c, R. Cimmaruta , J. Molloy h causing speciation in the marine environment. For A. Sanjuan k , S.A. Iversen d example, high potential dispersal may not translate to e , G. Nascetti , A.S. Comesa , 2002), there is , A.T. Santos d f high levels of realized gene flow. We mayet also al. gain a , A.L. Pinto , K. MacKenzie d c b Instituto Espa˜ b na˜ e insight into why there is high species diversity in School of BiologicalInstituto Sciences de (Zoology),Investiga¸ The University of, Aberdeen,C. Stransky Tillydrone Avenue,b Aberdeen AB24 2TZ, UK , G. Dahle Department of Ecology and Sustainable Economicnol Development, de Oceanograf´ Tuscia University, Via S. Giovanni Decollato,, R. Quinta 1, 01100 Viterbo,c Italy taxonomic groups with high dispersal potential. l , A. Magoulas f Although the rockfishes (Scorpaenidae: . Two investiga- fi Conserv Genet (2009) 10:1969–1972 cao das Pescas e do Mar, Av. Brasilia, 1400, C. Lisboa, Zimmermann Portugal b , , n tuna ıa, P.O. Box 240, 39080 Santander, Spain , P. Ramos i ) that waset al. DOI 10.1007/s10592-009-9870-8e Facultade de Biolox´ , considered an ancient species flock (Johns & Avise, 1998) m b Sebastomus Spatio-temporal population structuring and genetic f , g Institute of Marine Research, P.O. Box 1870, Nordnes, N-5817 Bergen, Norway with a high potential for dispersal (through a pelagic Instituto Espa˜ ıa, Edificio de Ciencias, UniversidadeIntroduction de Vigo, E-36200 Vigo, Spain (1999a) found recent speciation between TECHNICALi h Facultade NOTE de Ciencias de Lisboa (IO/DBA), Bloco C-2, Campo Grande, 1749-016 Lisboa, Portugal stage lasting 2–5 months; Love Sebastes miniatus j DepartmentHellenic of Public Centre Health for Sciences,Marine Research, Sectionnol de of Oceanograf´Institute Parasitology, of Marine “Sapienza” Biology and University Genetics, of P.O. Rome, Box piazzale 2214, GR Aldo 710 Moro 013 Iraklio, n Greece et al. d,3, Contemporary and evolutionary time-scale factors such evidence of recent speciation within the genus. Rocha- diversity retention in depleted Atlantic Blue c ıa, Avda. Tres de Mayo 73, 38005 Santa Cruz de Tenerife, Spain b , Massimo Sella Olivares , Lorenzo Zane as current or wind patterns, geographical barriers, 1471 Mar Biol b sister-taxa in the subgenus b , Alessia Cariani l Bundesforschungsanstalt f¨ demographic characteristics, physical changes in the of the MediterraneanDOI 10.1007/s00227-010-1419-3 Sea, Ilaria Milano m k The Marine Institute, Parkmore Industrial Estate, Galway, Ireland b,1,2, Giorgia Ferrara IsolationBundesforschungsanstalt and characterization f¨ of microsatelliteenvironment, or a combination markers of these, factors can act tions within rockfish species found cryptic speciation a,1 , Monica Landi b,4 ur Fischerei, Institut f¨ toSebastes reduce gene flow schlegeli among populations throughout a within vermilion rockfish ( ORIGINAL PAPER Giulia Riccioni a bDepartment of Experimental EvolutionaryAbstract Biology, Universityfor the of Bologna, heavily exploitedur Fischerei, Institut f¨ rockfish species’ range (Avise, 1994). In marine systems,spp. reduc- caused by difference in depth distribution (Hyde , and Fausto Tinti dInstitute Center for Marine Research, 52210 Rovinj, Croatia ur Seefischerei, Palmaille 9, D-22767 Hamburg, GermanySebastes Guido Barbujani ur Ostseefischerei, Alter Hafention S¨ or elimination in gene flow may lead to genetic 2008) and a similar pattern of sympatric distribution of Horse mackerel stock identificationand cross-species was carried out with the aimamplification of obtaining management inunits four that weredifferentiation relatedmeaningful biological or speciation entities and even within species with distinct genetic populations of Pacific ocean perch aDepartment of Biologyc and Evolution, University of Ferrara, 44100 Ferrara, Italy; thus improving the management of the resource. The stock identification was made by integrating both established and innovative approaches◦ 5, 00185 such Rome, Italy Department of Biology, University of Padova, 35121 Padova, Italy; and long pelagic stages, especially if populations are separated 40126 Bologna, Italy; Life history, ecology and the bi as genetic markers (allozymes, mitochondrial DNA, microsatellite DNA and SSCP on nuclear DNA),Æ morphometry,u 2, D-18069 parasites Rostock, as biological Germany tags, Jungfi Youn Park Æ Mi-Jung Kim (formerly Istituto Italo-Germanicobreaks among di Biologia Marina/Deutsch-Italienisches 15 species of Paci Institutogeography für Meersbiologie, of strong Rovigno, Italy) geneticand life history traits (growth,Hye reproduction Suck An and distribution),Æ sh- within the EU-funded HOMSIR project. The samplinginto different covered almost ecological the whole regions. Selective forces can also reproduction, high fecundity,distribution and high range mortality of horse mackerelEun of larval Young through stages Lee 20 samplingÆ Kyung localities Kil inKim Northeast Atlantic and Mediterranean Sea.lead Horse to mackerel genetic showed structure low or speciation in marine taxa Edited by Barbara Block, Stanford University, Stanford, CA, and accepted by theW Editorial Board December 1, 2009 (received for review July 24, 2009) with a long pelagic stage only if it is strong enough to c rock(reviewedWsh, in 14, 15). Nonetheless,levels of genetic tagging differentiation, experiments stable genetic and structure over the study time and high levels of genetic variability. However, several approache Arjun Sivasundar · Stephen R. Palumbifish. In this study, Sebastes (morphometrics and parasites) support the separation between the Atlantic Ocean and the Mediterranean Sea in horse mackerelcounteract populations, the homogenizing effect of gene flow. The Fishery genetics have greatly changed our understanding of ), an ery data analyses have unraveled an unexpected and complex although the most western Mediterranean area could also be mixed with the Atlantic populations. In the Northeast Atlantic,evaluation various stocks of the can begenetic relationship among populations Thunnus thynnus interplay of ecological, behavioral, and reproductive factors that Martha O. Burford, 208 Fernow Hall, Cornell(2009)University, 1471–1486 population dynamics and structuringfin tuna in marine (ABFT, 22 could affect the spatialdistinguished and temporal mainly population based on morphometrics, dynamics parasitesat thefiedtwo and life history traits: a “southern” stock is distributed along the West Atlantic coast of we show that the Atlantic Blue the Iberian Peninsula south to Cape Finisterre (NW Spain); a “western” stock, along the west coast of Europe from Cape Finisterre to Norway and large scale (11, 16). Microchemical signatures inReceived: otoliths 19 of February 2009 / Accepted: 24 February 2009 / Published online: 7 March 2009Correspondence: oceanic predatory species exhibiting highly migratory behavior, the “North Sea” stock. These results implied the revision of the boundaries of the southern and western stocks as previously defined.Ithaca, Results NY 14853, also USA. J. EVOL.2009 BIOL. EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY yearlings (i.e., young-of-the-year) unequivocallyÓ Springer identi Science+Business Media B.V. 2009 ª large population size, and highficant potential genetic fordifferences dispersal over during space early and suggested that adult horse mackerel could migrate through different areas following the west coasts in the Northeast Atlantic (i.e. betweenTel.: +1831 Celtic 419 7586; fax: +1 831 459 3383; e-mail: [email protected] life stages, displays signi n = main spawning areasSeas [i.e., and northernthe Mediterranean North Sea). Horse Sea mackerel for the from Eastern the Mauritanian coast is distinguished by its high growth rate and high batchelucidating fecundity. and Based monitoring the effect of such activities on fine and large scales of variation.256) Weand compared historical ( n = Atlantic population,on the the results Gulf from of morphometricMexico for theanalysis Western and the use Atlantic of parasites as biological tags, the horse mackerel population in the Mediterranean Sea2009 is THE AUTHOR.1993). Therefore, in recent years, the time, both at theReceived: 15 April 2009 / Accepted: 2 March 2010 Abstract Here we report development and characteriza- wild stocksª (FAO population (13)].sub-structured Because of into high at least rates three of main natal areas: homing western, of central and eastern Mediterranean. In this contribution,Sebastes we have integrated the fundamenta microsatellite© variation Springer-Verlag of contemporary 2010 ( tion of 14 polymorphic microsatellite loci from extent of stockingJOURNAL impacts COMPILATION upon indigenous populations has spawning adultsfindings to their of native different areas approaches (95.8% showing for thatthe the Medi- holistic approach is the appropriate way to identify horse mackerel stocks, on covering multiple 99) biological samples of ABFTs of the central-western Mediterra-ficit sug- . Polymorphism at these loci revealed from 3 to 23 terranean Sea andaspects 99.3% of the forbiology the of Gulf the species of Mexico) and reducingschlegel and the limited type I error and in stock identification. been a focus of attention from viewpointss of conservation nean Sea, theAbstract latter dating back to the early 20th century. Measures Strong genetic change over short spatial scales more complex© movements 2007 Elsevier B.V.in sexually Allficant rights maturegeneticreserved. ABFTsdivergencealleles. The(11, observed at17), both the heterozygosity ranged from 0.34 to and management for this species. However, to date little is of genetic differentiationis surprising among and a marine general species heterozygote with high dispersal de documenttwo populationsa wide variety showof patterns signi in gene 1.00, and the expected heterozygosity ranged from 0.31 to known about genetic diversity and population differentia- gest that differencespotential. existConcordant among breaks population among samples,several species both signals now Keywords: Trachurus trachurus –80 years ago. Thus, ABFTs do not represent a single panmic- ing thatmicrosatellite interaction of (12) individual and mtDNA species (18)traitsX loci. suchThe as 0.95. two ABFT No linkage pop- disequibrium was found. Two loci were tion of this species. Information regarding population and 96 a role for geographic barriers to dispersal. Along the coast ow, suggest- P \ 0.01). The 14 loci settlementulations behavior differ with in size,environmental with the eastern factors populationsuch as significantly approximately deviated from HWE ( structure, levels of gene flow and genetic diversity within tic populationof California, in the Mediterranean such breaks have Sea. not Statistics been seen designed across the to infer ; Stock identity; Holistic approach; Northeast Atlantic; MediterraneanSebastes Sea; Naturalspecies marks; and Life history12 traits oceanography10 times can as strongly large as impact the western population population structure. (19). Both are suf- changes in populationbiogeographic size, barrier both of from Point current Conception, and pastbut other genetic poten- var- ∗ Correspondingfishing author. and Tel.:are +34considered 942291060; fax: depleted,were +34 942275072. also surveyed consistent in four other and among populations of species harvested for com- iation, suggesttial geographic that some boundaries Mediterranean have been ABFT surveyed populations, less often. fering from overE-mail address: loci successfully amplified, where allelic diversity ranged mercial purposes can provide useful information for with the continuous decline of the spawning stock biomass although stillWe nottested severely for strong-population reduced in their structure genetic in potential,11 species of might [email protected] from highly polymorphic to monomorphic. These results developing conservation and management plans. S. schlegeli Introduction(which, in0165-7836/$ the eastern – see front stock, matter is © now 2007 Elsevier at 40% B.V. of All the rights 1970s reserved. levels), l have sufferedSebastes from sampled demographic across declines. two regions The short-term containing estimates potential doi: fishing mortality rate of age classdemonstrate 8 and older these indi- microsatellite markers can be used for Although six microsatellite markers from ), a set with the high10.1016/j.fishres.2007.09.022 (P. Abaunza). 2005 of effectivedispersal population barriers, size and= are 500)conducted straddled indicated a meta-analysis on to the maintain minimum including genetic threshold diver- the study of intra- and inter-specific genetic diversity. have been already reported by Yoshida et al. ( (effectivefour population additional sizespecies. We show two strong breaks north For many viduals,marine species, and with larval modeling dispersal predictions is a critical part (16, 19, 20). of migration ability, and life history di fi of molecular markers are needed for various other appli- sity and evolutionaryof Monterey Bay, potential spanning across an oceanographic several generations gradient and in The complex population dynamicsner exhibited scale in theby ABFTs Mediterranean at the Rockfish species can dramatically a Verences between Keywords Sebastes schlegel Á Á cations, from further population studies to pedigree naturalan populations. upwelling jet. Moderate genetic structure is just as com- large scale is alsoV apparent at a –23). Genetic Cross-amplification | large pelagicgenetic di V ect gene Xow. Investigations of Microsatellites markers analysis. In this work, we isolated 14 novel microsatellite mon in the north as it is in the south,| genetic across structure the biogeo- erencesSea (16). among Size-dependent marine populations movements have been and spawning in different Á , and represented their evaluation effective population size widely used to gauge levels of dispersal, which often scale S. schlegeli ancientgraphic DNA | break at Point Conception. Gene areas and periods have been documented (15, 21 markers from National Oceanic and Atmospheric Administration with larval traits such as pelagic duration (e.g. Berger fishes higherThunnus among thynnus deep-water species, but theseX owconclusions is generally are variation among three geographical samples suggested that at for cross-species amplification in four other related con- | Bohonak confounded by phylogeny. Species in the subgenus 1999least; Marko two subpopulations inhabit and1973 persist; Introduction over short time generic species. duration is short or absent2004 have). often Species been for found which to larval have ) values within the Med- osomus have higher structure than thoseSebast- in the subgenus periods (3 years) in the western and easternST Mediterranean Sea, We developed a partial genomic library enriched for CA ith an impressive amount of data accumulated in the lastfistrongsh pop- genetic structure among invertebrates’s genetic variance (McMillan (F , belonging to the family Pteropodus10–15 years,, despite genetic having studies larvae withhave longer greatly pelagic changed our yielding Wright Rockfish Sebastes schlegeli repeats as described in the protocol of Hamilton et al. W et al. 1992; Hellberg phases. Di Verences in settlement behavior in the face of iterranean1994, Sea1996 between 0.0007 and 0.0087 (12, 24). In this study, ) with a slight modification using prehybridization understanding of the ecology and evolution of marine 1987; Doherty et al. ) and Wshes (e.g. Waples Sebastinae and an important commercial fish in Korea, is (1999 ocean currents might we started1995 from a more thorough sampling of Mediterranean 1999). Genomic DNA help explain these di 2006 ; Riginos 2001 one of the species for which artificial reproduction and PCR amplification (Gardner et al. ulationssimilar by species showing across evidence the same of coastal complex environment, geneticVerences. structure weAcross at the ). However,ABFTs unexpectedly in space strong and structure time.; Along Purcell has also with et al. an extensive spatial sam- S. schlegel been demonstrated for some species that are presumed to spatial and temporal scales of variation. This is especially true for pling of contemporary ABFTs carried out fromcultivation 1999 to have 2007 intensively in been made throughout Korean was extracted from each fin tissue sample of fish species with high mobility, high potential for dispersal duringhave long distance dispersal potential (e.g. Reeb et al. the central-western Mediterranean (CWM),coastal we also areas had to access increaseFig. S1 the). harvest yield since the early captured in western coast of Korea using). TNES-Urea DNA was simulta- fish populations, both for2000 neutral; Barber et al. 1996 egg and larval stages, and large population sizes (1, 2). Accurate 2002 1990s. A stock enhancement program through the release buffer method (Asahida et al. RsaI, NheI Uncovering the reasonsto historical for; strong Burford ABFT genetic and specimens Bernardi breaks in such collected by one of the authors AluI, estimatesCommunicated of genetic by M. I. Taylor. variation in 2008). of hatchery-raised juveniles into natural environments has neously digested with restriction enzymes species can potentially(M.S.) reveal in the a great CWM deal tuna about traps larval between 1911 and 1926 ( and adaptive loci, can also suggest unique strategies for stock been practiced since the middle 1990s. In 2007, approxi- and HhaI (New England Biolabs, Bervery, MA, USA). A. Sivasundar · S. R. Palumbi –5). The assessmentmechanisms of that limit dispersal. management and conservationfishery resources of evolutionary (3 potential in mately two million seeds were released. In stock DNA fragments ranging from 300 to 800 bp were isolated severelyDepartment exploited of Biological Sciences, Hopkins Marine Station, Some of the clearest explanations of strong genetic Stanford University, 120 Oceanview Boulevard, breaks derive from theAuthor observation contributions: that M.L., in some G.B, and cases, F.T. designed these research;enhancement M.L., G.F., I.M., A.C., programs, and M.S. the genetic characterization of the and ligated to double-stranded linker-adapted primers populationW dynamics, environmentallyfish is crucial driven forchanges, both stock and levels man- Paci c Grove, CA 93950, USA breaks are concordantperformed with strong research; biogeographic G.R., M.L., G.F., bound- and L.Z. analyzed data; and G.R., G.F., L.Z., G.B, and (SNX/SNX rev linker sequences). Linker-ligated DNA F.T. wrote the paper. stocking species used should be assessed in view of of exploitation in large pelagic flict of interest. A. Sivasundar ( fisheries stillaries. remain Taxa the as diverse as coastal birds, tortoises, fragments were then amplified using single-stranded linker- agement and&) conservation of marine ecosystems dominated by The authors declare no con Division of Aquatic Ecology, invertebrates show strong geographic di W K. K. Kim fi sh and M.-J. Kim E. Y. Lee adapted primer (SNX) as polymerase chain reaction 0- Institutethese of oceanic Ecology and top Evolution, predators University (6). Although of Bern, ndings This article is a PNAS DirectV Submission. B.B. is a guest editor invited by the& Editorial) J. Y. Board. Park – Á Á the southeastern coast of the United States erentiation (Avise along H. S. An ( Á Á primer. Biotinylated dinucleotide repeat sequences [5 Baltzerstrassechief source 6, 3012 of Bern, data Switzerland forfi assessing–10), spatiotemporal whenever possible, population their 1G.R. and M.L. contributed equally to this work. Biotechnology Research Institute, National Fisheries Research 2002)] were hybridized to sh (7 fi 1996). Other cases of the con 1992 e-mail: [email protected] shery-independent approaches, 2 X , (CA)12GCTTGA-biotin (Li et al. dynamics of these graphic breaks in the oceansPresent have address:uence been of Department foundgenetic in and ofIndonesia, Biology, biogeo- University of Minho,and Development Campus de Gualtar, Institute, 4710 Busan 619-705, Korea should be compared with those of the western Mediterranean,057 Braga,the East Portugal. Paci e-mail: [email protected] such as genetic, electronic, and microchemical tagging experiments 3Deceased April 9, 1959.Wc and the Red Sea 123 –13), to have more accurate data on the key features of pop- 4 (11 ) is a large To whom correspondence should be addressed at: Department of Experimental Evolu- Thunnus thynnus ulation dynamics, suchfi asn tuna spawning (ABFT, and migrations (10). tionary Biology, University of Bologna, via Selmi 3, 40126 Bologna, Italy. E-mail: fausto. The Atlantic Blue [email protected]. www.pnas.org/cgi/content/full/ fish exploiting the pelagic ecosystems of the North 123 top-predator This article contains supporting. information online at Atlantic Ocean and Mediterranean Sea. Much like the other large 0908281107/DCSupplemental tunas, the ABFT displays highly migratory behavior, with docu- mented transoceanic and large-scale movements for feeding and no. 5 www.pnas.org/cgi/doi/10.1073/pnas.0908281107 | vol. 107 | PNAS | February 2, 2010 2102–2107 | Data doi: 10.1111/j.1420-9101.2009.01760.x ),

Sebastes mystinus • Microsatellite diversity

Demographic history, geographical distribution and reproductive isolation of distinct lineages of blue rockfish ( – 202 studies of 140 species a marine fish with a high dispersal potential ) are good taxa to examine speciation

M. O. BURFORD Sebastes mystinus described previously and use Department of Ecology and Evolutionary Biology, University of CaliforniaAbstract Santa Cruz, Santa Cruz, CA, USA Understanding the barriers to genetic exchangeS. in mystinus taxonomic groups that have a high dispersal potential will provide critical information on speciation in range revealed a northerly and general. Blue rockfish ( because they are nonmigratory inhabitants of shallow rocky reef habitats S. mystinus – Number of alleles (A) along the eastern North Pacific with a pelagic larval stage lasting 3–5 months. Keywords: Available online at www.sciencedirect.comThe goal of this study was to analyse the evolutionary history and distribution patterns of different lineages within admixture; this information to understand the speciation process in this group of high assignment test; dispersal fish. The molecular data derived from specimens sampled over microsatellite loci; approximately 1650 km of the mismatch distribution;Fisheries Research 89 (2008) 196–209 southerly distribution for the two lineages. Almost equal frequencies of both Stock identity of horsemtDNA mackerelcontrol region; ( lineages occurred at centrally located sample locations, with evidence of population expansion; reproductive isolation between the lineages. A demographic analysis showed reproductive isolation; Atlantic and Mediterranean Sea: Integrating thethat results the two fromlineages diverged, suggest and experienced both lineages sudden diverged expansion in allopatry. prior to the speciation. last glacial maximum, which affected the observed pattern of genetic structure. The spatialS. mystinus distribution, demographic history and degree of genetic Trachurus trachurusdistinctiveness found from the genetic analysis, despite the high potential for P. Abaunza different stock identification approachesdispersal in a , ) are M.T. Garc ∗, A.G. Murta ) in the Northeastor distinct lineages in areas where divergent lineages ´ıa Santamar b Sebastes S. Mattiucci , N. Campbell overlap and where only one lineage is found can improve ´ıa g our understanding of the evolutionary forces and events j , L.S. Gordo c, R. Cimmaruta , J. Molloy h causing speciation in the marine environment. For A. Sanjuan k , S.A. Iversen d example, high potential dispersal may not translate to e , G. Nascetti , A.S. Comesa , 2002), there is , A.T. Santos d f high levels of realized gene flow. We mayet also al. gain a , A.L. Pinto , K. MacKenzie d c b Instituto Espa˜ b na˜ e insight into why there is high species diversity in School of BiologicalInstituto Sciences de (Zoology),Investiga¸ The University of, Aberdeen,C. Stransky Tillydrone Avenue,b Aberdeen AB24 2TZ, UK , G. Dahle Department of Ecology and Sustainable Economicnol Development, de Oceanograf´ Tuscia University, Via S. Giovanni Decollato,, R. Quinta 1, 01100 Viterbo,c Italy taxonomic groups with high dispersal potential. l , A. Magoulas f Although the rockfishes (Scorpaenidae: . Two investiga- fi Conserv Genet (2009) 10:1969–1972 cao das Pescas e do Mar, Av. Brasilia, 1400, C. Lisboa, Zimmermann Portugal b , , n tuna ıa, P.O. Box 240, 39080 Santander, Spain , P. Ramos i ) that waset al. DOI 10.1007/s10592-009-9870-8e Facultade de Biolox´ , considered an ancient species flock (Johns & Avise, 1998) m b Sebastomus Spatio-temporal population structuring and genetic f , g Institute of Marine Research, P.O. Box 1870, Nordnes, N-5817 Bergen, Norway with a high potential for dispersal (through a pelagic Instituto Espa˜ ıa, Edificio de Ciencias, UniversidadeIntroduction de Vigo, E-36200 Vigo, Spain (1999a) found recent speciation between TECHNICALi h Facultade NOTE de Ciencias de Lisboa (IO/DBA), Bloco C-2, Campo Grande, 1749-016 Lisboa, Portugal stage lasting 2–5 months; Love Sebastes miniatus j DepartmentHellenic of Public Centre Health for Sciences,Marine Research, Sectionnol de of Oceanograf´Institute Parasitology, of Marine “Sapienza” Biology and University Genetics, of P.O. Rome, Box piazzale 2214, GR Aldo 710 Moro 013 Iraklio, n Greece et al. d,3, Contemporary and evolutionary time-scale factors such evidence of recent speciation within the genus. Rocha- diversity retention in depleted Atlantic Blue c ıa, Avda. Tres de Mayo 73, 38005 Santa Cruz de Tenerife, Spain b , Massimo Sella Olivares , Lorenzo Zane as current or wind patterns, geographical barriers, 1471 Mar Biol b sister-taxa in the subgenus b , Alessia Cariani l Bundesforschungsanstalt f¨ demographic characteristics, physical changes in the of the MediterraneanDOI 10.1007/s00227-010-1419-3 Sea, Ilaria Milano m k The Marine Institute, Parkmore Industrial Estate, Galway, Ireland b,1,2, Giorgia Ferrara IsolationBundesforschungsanstalt and characterization f¨ of microsatelliteenvironment, or a combination markers of these, factors can act tions within rockfish species found cryptic speciation a,1 , Monica Landi b,4 ur Fischerei, Institut f¨ toSebastes reduce gene flow schlegeli among populations throughout a within vermilion rockfish ( ORIGINAL PAPER Giulia Riccioni a bDepartment of Experimental EvolutionaryAbstract Biology, Universityfor the of Bologna, heavily exploitedur Fischerei, Institut f¨ rockfish species’ range (Avise, 1994). In marine systems,spp. reduc- caused by difference in depth distribution (Hyde , and Fausto Tinti dInstitute Center for Marine Research, 52210 Rovinj, Croatia ur Seefischerei, Palmaille 9, D-22767 Hamburg, GermanySebastes Guido Barbujani ur Ostseefischerei, Alter Hafention S¨ or elimination in gene flow may lead to genetic 2008) and a similar pattern of sympatric distribution of Horse mackerel stock identificationand cross-species was carried out with the aimamplification of obtaining management inunits four that weredifferentiation relatedmeaningful biological or speciation entities and even within species with distinct genetic populations of Pacific ocean perch aDepartment of Biologyc and Evolution, University of Ferrara, 44100 Ferrara, Italy; thus improving the management of the resource. The stock identification was made by integrating both established and innovative approaches◦ 5, 00185 such Rome, Italy Department of Biology, University of Padova, 35121 Padova, Italy; and long pelagic stages, especially if populations are separated 40126 Bologna, Italy; Life history, ecology and the bi as genetic markers (allozymes, mitochondrial DNA, microsatellite DNA and SSCP on nuclear DNA),Æ morphometry,u 2, D-18069 parasites Rostock, as biological Germany tags, Jungfi Youn Park Æ Mi-Jung Kim (formerly Istituto Italo-Germanicobreaks among di Biologia Marina/Deutsch-Italienisches 15 species of Paci Institutogeography für Meersbiologie, of strong Rovigno, Italy) geneticand life history traits (growth,Hye reproduction Suck An and distribution),Æ sh- within the EU-funded HOMSIR project. The samplinginto different covered almost ecological the whole regions. Selective forces can also reproduction, high fecundity,distribution and high range mortality of horse mackerelEun of larval Young through stages Lee 20 samplingÆ Kyung localities Kil inKim Northeast Atlantic and Mediterranean Sea.lead Horse to mackerel genetic showed structure low or speciation in marine taxa Edited by Barbara Block, Stanford University, Stanford, CA, and accepted by theW Editorial Board December 1, 2009 (received for review July 24, 2009) with a long pelagic stage only if it is strong enough to c rock(reviewedWsh, in 14, 15). Nonetheless,levels of genetic tagging differentiation, experiments stable genetic and structure over the study time and high levels of genetic variability. However, several approache Arjun Sivasundar · Stephen R. Palumbifish. In this study, Sebastes (morphometrics and parasites) support the separation between the Atlantic Ocean and the Mediterranean Sea in horse mackerelcounteract populations, the homogenizing effect of gene flow. The Fishery genetics have greatly changed our understanding of ), an ery data analyses have unraveled an unexpected and complex although the most western Mediterranean area could also be mixed with the Atlantic populations. In the Northeast Atlantic,evaluation various stocks of the can begenetic relationship among populations Thunnus thynnus interplay of ecological, behavioral, and reproductive factors that Martha O. Burford, 208 Fernow Hall, Cornell(2009)University, 1471–1486 population dynamics and structuringfin tuna in marine (ABFT, 22 could affect the spatialdistinguished and temporal mainly population based on morphometrics, dynamics parasitesat thefiedtwo and life history traits: a “southern” stock is distributed along the West Atlantic coast of we show that the Atlantic Blue the Iberian Peninsula south to Cape Finisterre (NW Spain); a “western” stock, along the west coast of Europe from Cape Finisterre to Norway and large scale (11, 16). Microchemical signatures inReceived: otoliths 19 of February 2009 / Accepted: 24 February 2009 / Published online: 7 March 2009Correspondence: oceanic predatory species exhibiting highly migratory behavior, the “North Sea” stock. These results implied the revision of the boundaries of the southern and western stocks as previously defined.Ithaca, Results NY 14853, also USA. J. EVOL.2009 BIOL. EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY yearlings (i.e., young-of-the-year) unequivocallyÓ Springer identi Science+Business Media B.V. 2009 ª large population size, and highficant potential genetic fordifferences dispersal over during space early and suggested that adult horse mackerel could migrate through different areas following the west coasts in the Northeast Atlantic (i.e. betweenTel.: +1831 Celtic 419 7586; fax: +1 831 459 3383; e-mail: [email protected] life stages, displays signi n = main spawning areasSeas [i.e., and northernthe Mediterranean North Sea). Horse Sea mackerel for the from Eastern the Mauritanian coast is distinguished by its high growth rate and high batchelucidating fecundity. and Based monitoring the effect of such activities on fine and large scales of variation.256) Weand compared historical ( n = Atlantic population,on the the results Gulf from of morphometricMexico for theanalysis Western and the use Atlantic of parasites as biological tags, the horse mackerel population in the Mediterranean Sea2009 is THE AUTHOR.1993). Therefore, in recent years, the time, both at theReceived: 15 April 2009 / Accepted: 2 March 2010 Abstract Here we report development and characteriza- wild stocksª (FAO population (13)].sub-structured Because of into high at least rates three of main natal areas: homing western, of central and eastern Mediterranean. In this contribution,Sebastes we have integrated the fundamenta microsatellite© variation Springer-Verlag of contemporary 2010 ( tion of 14 polymorphic microsatellite loci from extent of stockingJOURNAL impacts COMPILATION upon indigenous populations has spawning adultsfindings to their of native different areas approaches (95.8% showing for thatthe the Medi- holistic approach is the appropriate way to identify horse mackerel stocks, on covering multiple 99) biological samples of ABFTs of the central-western Mediterra-ficit sug- . Polymorphism at these loci revealed from 3 to 23 terranean Sea andaspects 99.3% of the forbiology the of Gulf the species of Mexico) and reducingschlegel and the limited type I error and in stock identification. been a focus of attention from viewpointss of conservation nean Sea, theAbstract latter dating back to the early 20th century. Measures Strong genetic change over short spatial scales more complex© movements 2007 Elsevier B.V.in sexually Allficant rights maturegeneticreserved. ABFTsdivergencealleles. The(11, observed at17), both the heterozygosity ranged from 0.34 to and management for this species. However, to date little is of genetic differentiationis surprising among and a marine general species heterozygote with high dispersal de documenttwo populationsa wide variety showof patterns signi in gene 1.00, and the expected heterozygosity ranged from 0.31 to known about genetic diversity and population differentia- gest that differencespotential. existConcordant among breaks population among samples,several species both signals now Keywords: Trachurus trachurus –80 years ago. Thus, ABFTs do not represent a single panmic- ing thatmicrosatellite interaction of (12) individual and mtDNA species (18)traitsX loci. suchThe as 0.95. two ABFT No linkage pop- disequibrium was found. Two loci were tion of this species. Information regarding population and 96 a role for geographic barriers to dispersal. Along the coast ow, suggest- P \ 0.01). The 14 loci settlementulations behavior differ with in size,environmental with the eastern factors populationsuch as significantly approximately deviated from HWE ( structure, levels of gene flow and genetic diversity within tic populationof California, in the Mediterranean such breaks have Sea. not Statistics been seen designed across the to infer ; Stock identity; Holistic approach; Northeast Atlantic; MediterraneanSebastes Sea; Naturalspecies marks; and Life history12 traits oceanography10 times can as strongly large as impact the western population population structure. (19). Both are suf- changes in populationbiogeographic size, barrier both of from Point current Conception, and pastbut other genetic poten- var- ∗ Correspondingfishing author. and Tel.:are +34considered 942291060; fax: depleted,were +34 942275072. also surveyed consistent in four other and among populations of species harvested for com- iation, suggesttial geographic that some boundaries Mediterranean have been ABFT surveyed populations, less often. fering from overE-mail address: loci successfully amplified, where allelic diversity ranged mercial purposes can provide useful information for with the continuous decline of the spawning stock biomass although stillWe nottested severely for strong-population reduced in their structure genetic in potential,11 species of might [email protected] from highly polymorphic to monomorphic. These results developing conservation and management plans. S. schlegeli Introduction(which, in0165-7836/$ the eastern – see front stock, matter is © now 2007 Elsevier at 40% B.V. of All the rights 1970s reserved. levels), l have sufferedSebastes from sampled demographic across declines. two regions The short-term containing estimates potential doi: fishing mortality rate of age classdemonstrate 8 and older these indi- microsatellite markers can be used for Although six microsatellite markers from ), a set with the high10.1016/j.fishres.2007.09.022 (P. Abaunza). 2005 of effectivedispersal population barriers, size and= are 500)conducted straddled indicated a meta-analysis on to the maintain minimum including genetic threshold diver- the study of intra- and inter-specific genetic diversity. have been already reported by Yoshida et al. ( (effectivefour population additional sizespecies. We show two strong breaks north For many viduals,marine species, and with larval modeling dispersal predictions is a critical part (16, 19, 20). of migration ability, and life history di fi of molecular markers are needed for various other appli- sity and evolutionaryof Monterey Bay, potential spanning across an oceanographic several generations gradient and in The complex population dynamicsner exhibited scale in theby ABFTs Mediterranean at the Rockfish species can dramatically a Verences between Keywords Sebastes schlegel Á Á cations, from further population studies to pedigree naturalan populations. upwelling jet. Moderate genetic structure is just as com- large scale is alsoV apparent at a –23). Genetic Cross-amplification | large pelagicgenetic di V ect gene Xow. Investigations of Microsatellites markers analysis. In this work, we isolated 14 novel microsatellite mon in the north as it is in the south,| genetic across structure the biogeo- erencesSea (16). among Size-dependent marine populations movements have been and spawning in different Á , and represented their evaluation effective population size widely used to gauge levels of dispersal, which often scale S. schlegeli ancientgraphic DNA | break at Point Conception. Gene areas and periods have been documented (15, 21 markers from National Oceanic and Atmospheric Administration with larval traits such as pelagic duration (e.g. Berger fishes higherThunnus among thynnus deep-water species, but theseX owconclusions is generally are variation among three geographical samples suggested that at for cross-species amplification in four other related con- | Bohonak confounded by phylogeny. Species in the subgenus 1999least; Marko two subpopulations inhabit and1973 persist; Introduction over short time generic species. duration is short or absent2004 have). often Species been for found which to larval have ) values within the Med- osomus have higher structure than thoseSebast- in the subgenus periods (3 years) in the western and easternST Mediterranean Sea, We developed a partial genomic library enriched for CA ith an impressive amount of data accumulated in the lastfistrongsh pop- genetic structure among invertebrates’s genetic variance (McMillan (F , belonging to the family Pteropodus10–15 years,, despite genetic having studies larvae withhave longer greatly pelagic changed our yielding Wright Rockfish Sebastes schlegeli repeats as described in the protocol of Hamilton et al. W et al. 1992; Hellberg phases. Di Verences in settlement behavior in the face of iterranean1994, Sea1996 between 0.0007 and 0.0087 (12, 24). In this study, ) with a slight modification using prehybridization understanding of the ecology and evolution of marine 1987; Doherty et al. ) and Wshes (e.g. Waples Sebastinae and an important commercial fish in Korea, is (1999 ocean currents might we started1995 from a more thorough sampling of Mediterranean 1999). Genomic DNA help explain these di 2006 ; Riginos 2001 one of the species for which artificial reproduction and PCR amplification (Gardner et al. ulationssimilar by species showing across evidence the same of coastal complex environment, geneticVerences. structure weAcross at the ). However,ABFTs unexpectedly in space strong and structure time.; Along Purcell has also with et al. an extensive spatial sam- S. schlegel been demonstrated for some species that are presumed to spatial and temporal scales of variation. This is especially true for pling of contemporary ABFTs carried out fromcultivation 1999 to have 2007 intensively in been made throughout Korean was extracted from each fin tissue sample of fish species with high mobility, high potential for dispersal duringhave long distance dispersal potential (e.g. Reeb et al. the central-western Mediterranean (CWM),coastal we also areas had to access increaseFig. S1 the). harvest yield since the early captured in western coast of Korea using). TNES-Urea DNA was simulta- fish populations, both for2000 neutral; Barber et al. 1996 egg and larval stages, and large population sizes (1, 2). Accurate 2002 1990s. A stock enhancement program through the release buffer method (Asahida et al. RsaI, NheI Uncovering the reasonsto historical for; strong Burford ABFT genetic and specimens Bernardi breaks in such collected by one of the authors AluI, estimatesCommunicated of genetic by M. I. Taylor. variation in 2008). of hatchery-raised juveniles into natural environments has neously digested with restriction enzymes species can potentially(M.S.) reveal in the a great CWM deal tuna about traps larval between 1911 and 1926 ( and adaptive loci, can also suggest unique strategies for stock been practiced since the middle 1990s. In 2007, approxi- and HhaI (New England Biolabs, Bervery, MA, USA). A. Sivasundar · S. R. Palumbi –5). The assessmentmechanisms of that limit dispersal. management and conservationfishery resources of evolutionary (3 potential in mately two million seeds were released. In stock DNA fragments ranging from 300 to 800 bp were isolated severelyDepartment exploited of Biological Sciences, Hopkins Marine Station, Some of the clearest explanations of strong genetic Stanford University, 120 Oceanview Boulevard, breaks derive from theAuthor observation contributions: that M.L., in some G.B, and cases, F.T. designed these research;enhancement M.L., G.F., I.M., A.C., programs, and M.S. the genetic characterization of the and ligated to double-stranded linker-adapted primers populationW dynamics, environmentallyfish is crucial driven forchanges, both stock and levels man- Paci c Grove, CA 93950, USA breaks are concordantperformed with strong research; biogeographic G.R., M.L., G.F., bound- and L.Z. analyzed data; and G.R., G.F., L.Z., G.B, and (SNX/SNX rev linker sequences). Linker-ligated DNA F.T. wrote the paper. stocking species used should be assessed in view of of exploitation in large pelagic flict of interest. A. Sivasundar ( fisheries stillaries. remain Taxa the as diverse as coastal birds, tortoises, fragments were then amplified using single-stranded linker- agement and&) conservation of marine ecosystems dominated by The authors declare no con Division of Aquatic Ecology, invertebrates show strong geographic di W K. K. Kim fi sh and M.-J. Kim E. Y. Lee adapted primer (SNX) as polymerase chain reaction 0- Institutethese of oceanic Ecology and top Evolution, predators University (6). Although of Bern, ndings This article is a PNAS DirectV Submission. B.B. is a guest editor invited by the& Editorial) J. Y. Board. Park – Á Á the southeastern coast of the United States erentiation (Avise along H. S. An ( Á Á primer. Biotinylated dinucleotide repeat sequences [5 Baltzerstrassechief source 6, 3012 of Bern, data Switzerland forfi assessing–10), spatiotemporal whenever possible, population their 1G.R. and M.L. contributed equally to this work. Biotechnology Research Institute, National Fisheries Research 2002)] were hybridized to sh (7 fi 1996). Other cases of the con 1992 e-mail: [email protected] shery-independent approaches, 2 X , (CA)12GCTTGA-biotin (Li et al. dynamics of these graphic breaks in the oceansPresent have address:uence been of Department foundgenetic in and ofIndonesia, Biology, biogeo- University of Minho,and Development Campus de Gualtar, Institute, 4710 Busan 619-705, Korea should be compared with those of the western Mediterranean,057 Braga,the East Portugal. Paci e-mail: [email protected] such as genetic, electronic, and microchemical tagging experiments 3Deceased April 9, 1959.Wc and the Red Sea 123 –13), to have more accurate data on the key features of pop- 4 (11 ) is a large To whom correspondence should be addressed at: Department of Experimental Evolu- Thunnus thynnus ulation dynamics, suchfi asn tuna spawning (ABFT, and migrations (10). tionary Biology, University of Bologna, via Selmi 3, 40126 Bologna, Italy. E-mail: fausto. The Atlantic Blue [email protected]. www.pnas.org/cgi/content/full/ fish exploiting the pelagic ecosystems of the North 123 top-predator This article contains supporting. information online at Atlantic Ocean and Mediterranean Sea. Much like the other large 0908281107/DCSupplemental tunas, the ABFT displays highly migratory behavior, with docu- mented transoceanic and large-scale movements for feeding and no. 5 www.pnas.org/cgi/doi/10.1073/pnas.0908281107 | vol. 107 | PNAS | February 2, 2010 2102–2107 | Data doi: 10.1111/j.1420-9101.2009.01760.x ),

Sebastes mystinus • Microsatellite diversity

Demographic history, geographical distribution and reproductive isolation of distinct lineages of blue rockfish ( – 202 studies of 140 species a marine fish with a high dispersal potential ) are good taxa to examine speciation

M. O. BURFORD Sebastes mystinus described previously and use Department of Ecology and Evolutionary Biology, University of CaliforniaAbstract Santa Cruz, Santa Cruz, CA, USA Understanding the barriers to genetic exchangeS. in mystinus taxonomic groups that have a high dispersal potential will provide critical information on speciation in range revealed a northerly and general. Blue rockfish ( because they are nonmigratory inhabitants of shallow rocky reef habitats S. mystinus – Number of alleles (A) along the eastern North Pacific with a pelagic larval stage lasting 3–5 months. Keywords: Available online at www.sciencedirect.comThe goal of this study was to analyse the evolutionary history and distribution patterns of different lineages within admixture; this information to understand the speciation process in this group of high assignment test; dispersal fish. The molecular data derived from specimens sampled over microsatellite loci; approximately 1650 km of the mismatch distribution;Fisheries Research 89 (2008) 196–209 southerly distribution for the two lineages. Almost equal frequencies of both Stock identity of horsemtDNA mackerelcontrol region; ( lineages occurred at centrally located sample locations, with evidence of population expansion; reproductive isolation between the lineages. A demographic analysis showed reproductive isolation; – Heterozygosity (H ) Atlantic and Mediterranean Sea: Integrating thethat results the two fromlineages diverged, suggest and experienced both lineages sudden diverged expansion in allopatry. prior to the e speciation. last glacial maximum, which affected the observed pattern of genetic structure. The spatialS. mystinus distribution, demographic history and degree of genetic Trachurus trachurusdistinctiveness found from the genetic analysis, despite the high potential for P. Abaunza different stock identification approachesdispersal in a , ) are M.T. Garc ∗, A.G. Murta ) in the Northeastor distinct lineages in areas where divergent lineages ´ıa Santamar b, N. Campbell overlap and where only one lineage is found can improveSebastes S. Mattiucci g j ´ıa , L.S. Gordo c our understanding of the evolutionary forces and events , J. Molloy , R. Cimmaruta causing speciation in the marine environment. For A. Sanjuan k h , G. Nascetti, S.A. Iversen d example, high potential dispersal may not translate to e , A.S. Comesa , 2002), there is , A.T. Santos d f high levels of realized gene flow. We mayet also al. gain a , A.L. Pinto , K. MacKenzie d c b Instituto Espa˜ b na˜ e insight into why there is high species diversity in School of BiologicalInstituto Sciences de (Zoology),Investiga¸ The University of, Aberdeen,C. Stransky Tillydrone Avenue,b Aberdeen AB24 2TZ, UK , G. Dahle Department of Ecology and Sustainable Economicnol Development, de Oceanograf´ Tuscia University, Via S. Giovanni Decollato,, R. Quinta 1, 01100 Viterbo,c Italy taxonomic groups with high dispersal potential. l , A. Magoulas f Although the rockfishes (Scorpaenidae: . Two investiga- fi Conserv Genet (2009) 10:1969–1972 cao das Pescas e do Mar, Av. Brasilia, 1400, C. Lisboa, Zimmermann Portugal b , , n tuna ıa, P.O. Box 240, 39080 Santander, Spain , P. Ramos i ) that waset al. DOI 10.1007/s10592-009-9870-8e Facultade de Biolox´ , considered an ancient species flock (Johns & Avise, 1998) m b Sebastomus Spatio-temporal population structuring and genetic f , g Institute of Marine Research, P.O. Box 1870, Nordnes, N-5817 Bergen, Norway with a high potential for dispersal (through a pelagic Instituto Espa˜ ıa, Edificio de Ciencias, UniversidadeIntroduction de Vigo, E-36200 Vigo, Spain (1999a) found recent speciation between TECHNICALi h Facultade NOTE de Ciencias de Lisboa (IO/DBA), Bloco C-2, Campo Grande, 1749-016 Lisboa, Portugal stage lasting 2–5 months; Love Sebastes miniatus j DepartmentHellenic of Public Centre Health for Sciences,Marine Research, Sectionnol de of Oceanograf´Institute Parasitology, of Marine “Sapienza” Biology and University Genetics, of P.O. Rome, Box piazzale 2214, GR Aldo 710 Moro 013 Iraklio, n Greece et al. d,3, Contemporary and evolutionary time-scale factors such evidence of recent speciation within the genus. Rocha- diversity retention in depleted Atlantic Blue c ıa, Avda. Tres de Mayo 73, 38005 Santa Cruz de Tenerife, Spain b , Massimo Sella Olivares , Lorenzo Zane as current or wind patterns, geographical barriers, 1471 Mar Biol b sister-taxa in the subgenus b , Alessia Cariani l Bundesforschungsanstalt f¨ demographic characteristics, physical changes in the of the MediterraneanDOI 10.1007/s00227-010-1419-3 Sea, Ilaria Milano m k The Marine Institute, Parkmore Industrial Estate, Galway, Ireland b,1,2, Giorgia Ferrara IsolationBundesforschungsanstalt and characterization f¨ of microsatelliteenvironment, or a combination markers of these, factors can act tions within rockfish species found cryptic speciation a,1 , Monica Landi b,4 ur Fischerei, Institut f¨ toSebastes reduce gene flow schlegeli among populations throughout a within vermilion rockfish ( ORIGINAL PAPER Giulia Riccioni a bDepartment of Experimental EvolutionaryAbstract Biology, Universityfor the of Bologna, heavily exploitedur Fischerei, Institut f¨ rockfish species’ range (Avise, 1994). In marine systems,spp. reduc- caused by difference in depth distribution (Hyde , and Fausto Tinti dInstitute Center for Marine Research, 52210 Rovinj, Croatia ur Seefischerei, Palmaille 9, D-22767 Hamburg, GermanySebastes Guido Barbujani ur Ostseefischerei, Alter Hafention S¨ or elimination in gene flow may lead to genetic 2008) and a similar pattern of sympatric distribution of Horse mackerel stock identificationand cross-species was carried out with the aimamplification of obtaining management inunits four that weredifferentiation relatedmeaningful biological or speciation entities and even within species with distinct genetic populations of Pacific ocean perch aDepartment of Biologyc and Evolution, University of Ferrara, 44100 Ferrara, Italy; thus improving the management of the resource. The stock identification was made by integrating both established and innovative approaches◦ 5, 00185 such Rome, Italy Department of Biology, University of Padova, 35121 Padova, Italy; and long pelagic stages, especially if populations are separated 40126 Bologna, Italy; Life history, ecology and the bi as genetic markers (allozymes, mitochondrial DNA, microsatellite DNA and SSCP on nuclear DNA),Æ morphometry,u 2, D-18069 parasites Rostock, as biological Germany tags, Jungfi Youn Park Æ Mi-Jung Kim (formerly Istituto Italo-Germanicobreaks among di Biologia Marina/Deutsch-Italienisches 15 species of Paci Institutogeography für Meersbiologie, of strong Rovigno, Italy) geneticand life history traits (growth,Hye reproduction Suck An and distribution),Æ sh- within the EU-funded HOMSIR project. The samplinginto different covered almost ecological the whole regions. Selective forces can also reproduction, high fecundity,distribution and high range mortality of horse mackerelEun of larval Young through stages Lee 20 samplingÆ Kyung localities Kil inKim Northeast Atlantic and Mediterranean Sea.lead Horse to mackerel genetic showed structure low or speciation in marine taxa Edited by Barbara Block, Stanford University, Stanford, CA, and accepted by theW Editorial Board December 1, 2009 (received for review July 24, 2009) with a long pelagic stage only if it is strong enough to c rock(reviewedWsh, in 14, 15). Nonetheless,levels of genetic tagging differentiation, experiments stable genetic and structure over the study time and high levels of genetic variability. However, several approache Arjun Sivasundar · Stephen R. Palumbifish. In this study, Sebastes (morphometrics and parasites) support the separation between the Atlantic Ocean and the Mediterranean Sea in horse mackerelcounteract populations, the homogenizing effect of gene flow. The Fishery genetics have greatly changed our understanding of ), an ery data analyses have unraveled an unexpected and complex although the most western Mediterranean area could also be mixed with the Atlantic populations. In the Northeast Atlantic,evaluation various stocks of the can begenetic relationship among populations Thunnus thynnus interplay of ecological, behavioral, and reproductive factors that Martha O. Burford, 208 Fernow Hall, Cornell(2009)University, 1471–1486 population dynamics and structuringfin tuna in marine (ABFT, 22 could affect the spatialdistinguished and temporal mainly population based on morphometrics, dynamics parasitesat thefiedtwo and life history traits: a “southern” stock is distributed along the West Atlantic coast of we show that the Atlantic Blue the Iberian Peninsula south to Cape Finisterre (NW Spain); a “western” stock, along the west coast of Europe from Cape Finisterre to Norway and large scale (11, 16). Microchemical signatures inReceived: otoliths 19 of February 2009 / Accepted: 24 February 2009 / Published online: 7 March 2009Correspondence: oceanic predatory species exhibiting highly migratory behavior, the “North Sea” stock. These results implied the revision of the boundaries of the southern and western stocks as previously defined.Ithaca, Results NY 14853, also USA. J. EVOL.2009 BIOL. EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY yearlings (i.e., young-of-the-year) unequivocallyÓ Springer identi Science+Business Media B.V. 2009 ª large population size, and highficant potential genetic fordifferences dispersal over during space early and suggested that adult horse mackerel could migrate through different areas following the west coasts in the Northeast Atlantic (i.e. betweenTel.: +1831 Celtic 419 7586; fax: +1 831 459 3383; e-mail: [email protected] life stages, displays signi n = main spawning areasSeas [i.e., and northernthe Mediterranean North Sea). Horse Sea mackerel for the from Eastern the Mauritanian coast is distinguished by its high growth rate and high batchelucidating fecundity. and Based monitoring the effect of such activities on fine and large scales of variation.256) Weand compared historical ( n = Atlantic population,on the the results Gulf from of morphometricMexico for theanalysis Western and the use Atlantic of parasites as biological tags, the horse mackerel population in the Mediterranean Sea2009 is THE AUTHOR.1993). Therefore, in recent years, the time, both at theReceived: 15 April 2009 / Accepted: 2 March 2010 Abstract Here we report development and characteriza- wild stocksª (FAO population (13)].sub-structured Because of into high at least rates three of main natal areas: homing western, of central and eastern Mediterranean. In this contribution,Sebastes we have integrated the fundamenta microsatellite© variation Springer-Verlag of contemporary 2010 ( tion of 14 polymorphic microsatellite loci from extent of stockingJOURNAL impacts COMPILATION upon indigenous populations has spawning adultsfindings to their of native different areas approaches (95.8% showing for thatthe the Medi- holistic approach is the appropriate way to identify horse mackerel stocks, on covering multiple 99) biological samples of ABFTs of the central-western Mediterra-ficit sug- . Polymorphism at these loci revealed from 3 to 23 terranean Sea andaspects 99.3% of the forbiology the of Gulf the species of Mexico) and reducingschlegel and the limited type I error and in stock identification. been a focus of attention from viewpointss of conservation nean Sea, theAbstract latter dating back to the early 20th century. Measures Strong genetic change over short spatial scales more complex© movements 2007 Elsevier B.V.in sexually Allficant rights maturegeneticreserved. ABFTsdivergencealleles. The(11, observed at17), both the heterozygosity ranged from 0.34 to and management for this species. However, to date little is of genetic differentiationis surprising among and a marine general species heterozygote with high dispersal de documenttwo populationsa wide variety showof patterns signi in gene 1.00, and the expected heterozygosity ranged from 0.31 to known about genetic diversity and population differentia- gest that differencespotential. existConcordant among breaks population among samples,several species both signals now Keywords: Trachurus trachurus –80 years ago. Thus, ABFTs do not represent a single panmic- ing thatmicrosatellite interaction of (12) individual and mtDNA species (18)traitsX loci. suchThe as 0.95. two ABFT No linkage pop- disequibrium was found. Two loci were tion of this species. Information regarding population and 96 a role for geographic barriers to dispersal. Along the coast ow, suggest- P \ 0.01). The 14 loci settlementulations behavior differ with in size,environmental with the eastern factors populationsuch as significantly approximately deviated from HWE ( structure, levels of gene flow and genetic diversity within tic populationof California, in the Mediterranean such breaks have Sea. not Statistics been seen designed across the to infer ; Stock identity; Holistic approach; Northeast Atlantic; MediterraneanSebastes Sea; Naturalspecies marks; and Life history12 traits oceanography10 times can as strongly large as impact the western population population structure. (19). Both are suf- changes in populationbiogeographic size, barrier both of from Point current Conception, and pastbut other genetic poten- var- ∗ Correspondingfishing author. and Tel.:are +34considered 942291060; fax: depleted,were +34 942275072. also surveyed consistent in four other and among populations of species harvested for com- iation, suggesttial geographic that some boundaries Mediterranean have been ABFT surveyed populations, less often. fering from overE-mail address: loci successfully amplified, where allelic diversity ranged mercial purposes can provide useful information for with the continuous decline of the spawning stock biomass although stillWe nottested severely for strong-population reduced in their structure genetic in potential,11 species of might [email protected] from highly polymorphic to monomorphic. These results developing conservation and management plans. S. schlegeli Introduction(which, in0165-7836/$ the eastern – see front stock, matter is © now 2007 Elsevier at 40% B.V. of All the rights 1970s reserved. levels), l have sufferedSebastes from sampled demographic across declines. two regions The short-term containing estimates potential doi: fishing mortality rate of age classdemonstrate 8 and older these indi- microsatellite markers can be used for Although six microsatellite markers from ), a set with the high10.1016/j.fishres.2007.09.022 (P. Abaunza). 2005 of effectivedispersal population barriers, size and= are 500)conducted straddled indicated a meta-analysis on to the maintain minimum including genetic threshold diver- the study of intra- and inter-specific genetic diversity. have been already reported by Yoshida et al. ( (effectivefour population additional sizespecies. We show two strong breaks north For many viduals,marine species, and with larval modeling dispersal predictions is a critical part (16, 19, 20). of migration ability, and life history di fi of molecular markers are needed for various other appli- sity and evolutionaryof Monterey Bay, potential spanning across an oceanographic several generations gradient and in The complex population dynamicsner exhibited scale in theby ABFTs Mediterranean at the Rockfish species can dramatically a Verences between Keywords Sebastes schlegel Á Á cations, from further population studies to pedigree naturalan populations. upwelling jet. Moderate genetic structure is just as com- large scale is alsoV apparent at a –23). Genetic Cross-amplification | large pelagicgenetic di V ect gene Xow. Investigations of Microsatellites markers analysis. In this work, we isolated 14 novel microsatellite mon in the north as it is in the south,| genetic across structure the biogeo- erencesSea (16). among Size-dependent marine populations movements have been and spawning in different Á , and represented their evaluation effective population size widely used to gauge levels of dispersal, which often scale S. schlegeli ancientgraphic DNA | break at Point Conception. Gene areas and periods have been documented (15, 21 markers from National Oceanic and Atmospheric Administration with larval traits such as pelagic duration (e.g. Berger fishes higherThunnus among thynnus deep-water species, but theseX owconclusions is generally are variation among three geographical samples suggested that at for cross-species amplification in four other related con- | Bohonak confounded by phylogeny. Species in the subgenus 1999least; Marko two subpopulations inhabit and1973 persist; Introduction over short time generic species. duration is short or absent2004 have). often Species been for found which to larval have ) values within the Med- osomus have higher structure than thoseSebast- in the subgenus periods (3 years) in the western and easternST Mediterranean Sea, We developed a partial genomic library enriched for CA ith an impressive amount of data accumulated in the lastfistrongsh pop- genetic structure among invertebrates’s genetic variance (McMillan (F , belonging to the family Pteropodus10–15 years,, despite genetic having studies larvae withhave longer greatly pelagic changed our yielding Wright Rockfish Sebastes schlegeli repeats as described in the protocol of Hamilton et al. W et al. 1992; Hellberg phases. Di Verences in settlement behavior in the face of iterranean1994, Sea1996 between 0.0007 and 0.0087 (12, 24). In this study, ) with a slight modification using prehybridization understanding of the ecology and evolution of marine 1987; Doherty et al. ) and Wshes (e.g. Waples Sebastinae and an important commercial fish in Korea, is (1999 ocean currents might we started1995 from a more thorough sampling of Mediterranean 1999). Genomic DNA help explain these di 2006 ; Riginos 2001 one of the species for which artificial reproduction and PCR amplification (Gardner et al. ulationssimilar by species showing across evidence the same of coastal complex environment, geneticVerences. structure weAcross at the ). However,ABFTs unexpectedly in space strong and structure time.; Along Purcell has also with et al. an extensive spatial sam- S. schlegel been demonstrated for some species that are presumed to spatial and temporal scales of variation. This is especially true for pling of contemporary ABFTs carried out fromcultivation 1999 to have 2007 intensively in been made throughout Korean was extracted from each fin tissue sample of fish species with high mobility, high potential for dispersal duringhave long distance dispersal potential (e.g. Reeb et al. the central-western Mediterranean (CWM),coastal we also areas had to access increaseFig. S1 the). harvest yield since the early captured in western coast of Korea using). TNES-Urea DNA was simulta- fish populations, both for2000 neutral; Barber et al. 1996 egg and larval stages, and large population sizes (1, 2). Accurate 2002 1990s. A stock enhancement program through the release buffer method (Asahida et al. RsaI, NheI Uncovering the reasonsto historical for; strong Burford ABFT genetic and specimens Bernardi breaks in such collected by one of the authors AluI, estimatesCommunicated of genetic by M. I. Taylor. variation in 2008). of hatchery-raised juveniles into natural environments has neously digested with restriction enzymes species can potentially(M.S.) reveal in the a great CWM deal tuna about traps larval between 1911 and 1926 ( and adaptive loci, can also suggest unique strategies for stock been practiced since the middle 1990s. In 2007, approxi- and HhaI (New England Biolabs, Bervery, MA, USA). A. Sivasundar · S. R. Palumbi –5). The assessmentmechanisms of that limit dispersal. management and conservationfishery resources of evolutionary (3 potential in mately two million seeds were released. In stock DNA fragments ranging from 300 to 800 bp were isolated severelyDepartment exploited of Biological Sciences, Hopkins Marine Station, Some of the clearest explanations of strong genetic Stanford University, 120 Oceanview Boulevard, breaks derive from theAuthor observation contributions: that M.L., in some G.B, and cases, F.T. designed these research;enhancement M.L., G.F., I.M., A.C., programs, and M.S. the genetic characterization of the and ligated to double-stranded linker-adapted primers populationW dynamics, environmentallyfish is crucial driven forchanges, both stock and levels man- Paci c Grove, CA 93950, USA breaks are concordantperformed with strong research; biogeographic G.R., M.L., G.F., bound- and L.Z. analyzed data; and G.R., G.F., L.Z., G.B, and (SNX/SNX rev linker sequences). Linker-ligated DNA F.T. wrote the paper. stocking species used should be assessed in view of of exploitation in large pelagic flict of interest. A. Sivasundar ( fisheries stillaries. remain Taxa the as diverse as coastal birds, tortoises, fragments were then amplified using single-stranded linker- agement and&) conservation of marine ecosystems dominated by The authors declare no con Division of Aquatic Ecology, invertebrates show strong geographic di W K. K. Kim fi sh and M.-J. Kim E. Y. Lee adapted primer (SNX) as polymerase chain reaction 0- Institutethese of oceanic Ecology and top Evolution, predators University (6). Although of Bern, ndings This article is a PNAS DirectV Submission. B.B. is a guest editor invited by the& Editorial) J. Y. Board. Park – Á Á the southeastern coast of the United States erentiation (Avise along H. S. An ( Á Á primer. Biotinylated dinucleotide repeat sequences [5 Baltzerstrassechief source 6, 3012 of Bern, data Switzerland forfi assessing–10), spatiotemporal whenever possible, population their 1G.R. and M.L. contributed equally to this work. Biotechnology Research Institute, National Fisheries Research 2002)] were hybridized to sh (7 fi 1996). Other cases of the con 1992 e-mail: [email protected] shery-independent approaches, 2 X , (CA)12GCTTGA-biotin (Li et al. dynamics of these graphic breaks in the oceansPresent have address:uence been of Department foundgenetic in and ofIndonesia, Biology, biogeo- University of Minho,and Development Campus de Gualtar, Institute, 4710 Busan 619-705, Korea should be compared with those of the western Mediterranean,057 Braga,the East Portugal. Paci e-mail: [email protected] such as genetic, electronic, and microchemical tagging experiments 3Deceased April 9, 1959.Wc and the Red Sea 123 –13), to have more accurate data on the key features of pop- 4 (11 ) is a large To whom correspondence should be addressed at: Department of Experimental Evolu- Thunnus thynnus ulation dynamics, suchfi asn tuna spawning (ABFT, and migrations (10). tionary Biology, University of Bologna, via Selmi 3, 40126 Bologna, Italy. E-mail: fausto. The Atlantic Blue [email protected]. www.pnas.org/cgi/content/full/ fish exploiting the pelagic ecosystems of the North 123 top-predator This article contains supporting. information online at Atlantic Ocean and Mediterranean Sea. Much like the other large 0908281107/DCSupplemental tunas, the ABFT displays highly migratory behavior, with docu- mented transoceanic and large-scale movements for feeding and no. 5 www.pnas.org/cgi/doi/10.1073/pnas.0908281107 | vol. 107 | PNAS | February 2, 2010 2102–2107 | 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

A = 16 New Zealand snapper He = 0.7 (Pagrus auratus)

A = 12

He = 0.8 Other Pagrus

Pinsky et al. 2014 Molecular Ecology Paired comparisons overfished vs. control

A50 = 10.2 A50 = 10.2 He = 0.736A = 10.2 H =50 0.736A = 10.2 e H =50 0.736 e A50 = 10.2 He = 0.736A = 10.2 H =50 0.736A = 10.2 e H =50 0.736 e A50 = 10.2 He = 0.736A = 10.2 H =50 0.736A = 10.2 e H =50 0.736 e A50 = 10.2 He = 0.736A = 10.2 A50 = 16.6 50 He = 0.736A = 10.2 A50 = 16.6 50 H = 0.846 He = 0.736 e A50 = 16.6 H = 0.846 He = 0.736 e A50 = 16.6 He = 0.846A = 16.6 H =50 0.846A = 16.6 e H =50 0.846 e A50 = 16.6 He = 0.846A = 16.6 H =50 0.846A = 16.6 e H =50 0.846 e A50 = 16.6 He = 0.846A = 16.6 H =50 0.846A = 16.6 n = 12 e H =50 0.846 e A50 = 16.6 He = 0.846 He = 0.846 DrumCynoscion ●

TunasScombridae ●

FloundersPleuronectidae ●

SeabreamPagrus ●

HerringsClupeidae ●

TurbotsScophthalmidae ●

CodsGadidae ●

RockfishesSebastes ●

GroupersSerranidae ●

SnappersLutjanus ●

JackTrachurus mackerels ●

SmeltsOsmeridae ●

−50 −25 0 25 50

%% difference More Alleles in in Overfished allelic richness

Pinsky et al. Molecular Ecology DrumCynoscion ●

TunasScombridae ●

FloundersPleuronectidae ●

SeabreamPagrus ●

HerringsClupeidae ●

TurbotsScophthalmidae ●

CodsGadidae ●

RockfishesSebastes ●

GroupersSerranidae ●

SnappersLutjanus ●

JackTrachurus mackerels ●

SmeltsOsmeridae ●

−50 −25 0 25 50

%% difference More Alleles in in Overfished allelic richness

Pinsky et al. Molecular Ecology DrumCynoscion ●

TunasScombridae ●

FloundersPleuronectidae ●

SeabreamPagrus ●

HerringsClupeidae ●

TurbotsScophthalmidae ●

CodsGadidae ●

RockfishesSebastes ●

GroupersSerranidae ●

SnappersLutjanus ●

JackTrachurus mackerels ●

SmeltsOsmeridae ●

−50 −25 0 25 50

%% difference More Alleles in in Overfished allelic richness

Pinsky et al. Molecular Ecology DrumCynoscion ●

TunasScombridae ●

FloundersPleuronectidae ●

SeabreamPagrus ●

HerringsClupeidae ●

TurbotsScophthalmidae Overfished● Overfished populations populations CodsGadidae ● have lower have higher RockfishesSebastes diversity ● diversity GroupersSerranidae ●

SnappersLutjanus ●

JackTrachurus mackerels ●

SmeltsOsmeridae ●

−50 −25 0 25 50

%% difference More Alleles in in Overfished allelic richness

Pinsky et al. Molecular Ecology DrumCynoscion ●

TunasScombridae ●

FloundersPleuronectidae ●

SeabreamPagrus ●

HerringsClupeidae ●

TurbotsScophthalmidae ●

CodsGadidae ●

RockfishesSebastes ●

GroupersSerranidae ●

SnappersLutjanus ●

JackTrachurus mackerels ●

SmeltsOsmeridae ●

−50 −25 0 25 50

%% difference More Alleles in in Overfished allelic richness

Pinsky et al. Molecular Ecology DrumCynoscion ●

TunasScombridae ● 9 of 12 groups FloundersPleuronectidae ● have lower SeabreamPagrus ● diversity in overfished HerringsClupeidae ● populations TurbotsScophthalmidae ●

CodsGadidae ●

RockfishesSebastes ●

GroupersSerranidae ●

SnappersLutjanus ●

JackTrachurus mackerels ●

SmeltsOsmeridae ●

−50 −25 0 25 50

%% difference More Alleles in in Overfished allelic richness

Pinsky et al. Molecular Ecology DrumCynoscion ●

TunasScombridae ●

FloundersPleuronectidae ●

SeabreamPagrus ●

HerringsClupeidae ●

TurbotsScophthalmidae ● CodsGadidae ● Average: RockfishesSebastes ●

GroupersSerranidae ● 12% lower

SnappersLutjanus ●

JackTrachurus mackerels ●

SmeltsOsmeridae ●

−50 −25 0 25 50

%% difference More Alleles in in Overfished allelic richness

Pinsky et al. Molecular Ecology 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