shallow population histories in deep evolutionary...

415

q 1998 The American Genetic Association 89:415–426

Shallow Population Histories in DeepEvolutionary Lineages of Marine Fishes:Insights From Sardines and Anchovies andLessons for ConservationW. S. Grant and B. W. Bowen

Most surveys of mitochondrial DNA (mtDNA) in marine fishes reveal low levels ofsequence divergence between haplotypes relative to the differentiation observedbetween sister taxa. It is unclear whether this pattern is due to rapid lineage sortingaccelerated by sweepstakes recruitment, historical bottlenecks in population size,founder events, or natural selection, any of which could retard the accumulationof deep mtDNA lineages. Recent advances in paleoclimate research prompt a re-examination of oceanographic processes as a fundamental influence on geneticdiversity; evidence from ice cores and anaerobic marine sediments documentstrong regime shifts in the world’s oceans in concert with periodic climaticchanges. These changes in sea surface temperatures, current pathways, upwellingintensities, and retention eddies are likely harbingers of severe fluctuations in pop-ulation size or regional extinctions. Sardines (Sardina, Sardinops) and anchovies(Engraulis) are used to assess the consequences of such oceanographic process-es on marine fish intrageneric gene genealogies. Representatives of these twogroups occur in temperate boundary currents on a global scale, and these regionalpopulations are known to fluctuate markedly. Biogeographic and genetic data in-dicate that Sardinops has persisted for at least 20 million years, yet the mtDNAgenealogy for this group coalesces in less than half a million years and points toa recent founding of populations around the rim of the Indian–Pacific Ocean. Phy-logeographic analysis of Old World anchovies reveals a Pleistocene dispersal fromthe Pacific to the Atlantic, almost certainly via southern Africa, followed by a veryrecent recolonization from Europe to southern Africa. These results demonstratethat regional populations of sardines and anchovies are subject to periodic extinc-tions and recolonizations. Such climate-associated dynamics may explain the lowlevels of nucleotide diversity and the shallow coalescence of mtDNA genealogies.If these findings apply generally to marine fishes, management strategies shouldincorporate the idea that even extremely abundant populations may be relativelyfragile on ecological and evolutionary time scales.

A recurring debate in evolutionary biologyis over the extent to which microevolution-ary processes operating within a species canbe extrapolated to explain macroevolution-ary differences among species . . .

Avise et al. (1987, p. 489)

To understand the dynamics of marinefish populations, researchers must identi-fy the conditions that regulate reproduc-tion, population growth, and persistence.On short (ecological) time scales, a vari-ety of factors, including nutrient cycles,food-chain processes, spawning, preda-tion, recruitment, and climate have beenproposed as primary regulators of abun-dance (Butler 1991; Parrish and Mallicoate1995; Smith et al. 1992; Watanabe and Ku-

roki 1997). Although several early hypoth-eses about population regulation are nowdiscounted on the basis of field studies,other hypotheses remain untested be-cause of the lack of an appropriate tool.Recent advances in sampling technologyand satellite imagery show considerablepromise, demonstrating, for example, thatin the California Current egg and larvalproduction is contingent on small upwell-ing plumes along the coast (Lo et al.1996).

One emerging generalization from mo-lecular analyses is that marine fishes areoften characterized by shallow populationgenetic architectures, even though geneticdivergence from sister taxa indicates sep-

From the Conservation Biology Division, NorthwestFisheries Science Center, NOAA, Seattle, Washington,and the Department of Fisheries and Aquatic Sciences,University of Florida, Gainesville, Florida. We thank A.Bass, A. Clark, and A. Garcia for technical support, andR. Leslie and A. Payne (Sea Fisheries Research Insti-tute, Cape Town, South Africa), T. Kobayashi (NationalResearch Institute of Fisheries Science, Yokohama, Ja-pan), S. Jablanski (SUDEPPE, Rio de Janeiro, Brazil),and J. Shaklee (CSIRO, Canberra, Australia) for gener-ously providing samples for the various studies re-viewed in this article. K. Bailey, J. Gold, S. Karl, T.Streelman, F. Utter, and R. Waples provided insightfulcomments on the manuscript. Genetic studies of sar-dines and anchovies were supported by the U.S. Na-tional Science Foundation and by the Foundation forResearch Development, Pretoria, South Africa. Addresscorrespondence to Dr. Grant, Northwest Fisheries Sci-ence Center, 2725 Montlake Boulevard East, Seattle, WA98112-2097, or e-mail: [email protected]. This paperwas delivered at a symposium entitled ‘‘Conservationand Genetics of Marine Organisms’’ sponsored by theAmerican Genetics Association at the University of Vic-toria, Victoria, BC, Canada, June 7, 1997.

416 The Journal of Heredity 1998:89(5)

Figure 1. Geographical distributions of sardines (Sardina, Sardinops) and anchovies (Engraulis) with 138C and258C isotherms (dashed lines).

arations of millions of years. In a review ofmitochondrial DNA (mtDNA) diversity inwidely distributed marine fishes, Shieldsand Gust (1995) noted a recurring patternof a single or a few prevalent haplotypeswith numerous rare haplotypes that wereone or two mutations removed from thecommon haplotype. These starlike phylog-enies characterize regional populations ofhaddock (Melanogrammus aeglefinus; Zwa-nenburg et al. 1992), Atlantic cod (Gadusmorhua; Carr and Marshall 1991; Smith etal. 1989), cape hake (Merluccius capensis;Becker et al. 1988), deepwater hake (M.paradoxus; Becker et al. 1988), Atlanticherring (Clupea harengus; Kornfield andBogdanowicz 1987), Pacific herring (C. pal-lasi; Schweigert and Withler 1990), reddrum (Sciaenops ocellatus; Gold et al.1993), black drum (Pogonias cromis; Goldet al. 1994), greater amberjack (Seriola du-merili; Richardson and Gold 1993), redsnapper (Lutjanus compechanus; Camperet al. 1993), Spanish sardine (Sardinella au-rita; Tringali and Wilson 1993), orangeroughy (Hoplostethus atlanticus; Baker etal. 1995; Ovenden et al. 1989; Smolenski etal. 1993), Atlantic capelin (Mallotus villo-sus; Dodson et al. 1991), albacore tuna(Thunnus alalunga; Graves and Dizon1989), and skipjack tuna (Katsuwonus pe-lamis; Graves et al. 1984). Shallow haplo-type divergences atop long lineages arealso clearly illustrated in Figures 4 and 5of Bermingham et al. (1997) for species ofdamselfish isolated about 3 million yearsago by the formation of the Panama isth-mus. Explanations for this widespread pat-tern include a large variance in reproduc-tive success that leads to the propagationof only a few haplotypes (Shields and Gust1995), overharvesting (Camper et al.1993), the physical nature of the pelagicrealm (Graves 1995), recent habitat reduc-tions (Shulman and Bermingham 1995),population bottlenecks (Gold et al. 1994),or other ‘‘demographic events’’ (Dodsonet al. 1991).

This phenomenon is also apparent insardines (Sardina, Sardinops) and ancho-vies (Engraulis). Both groups are globallydistributed in temperate zones and haverepresentative species or populations inmost of the world’s temperate boundarycurrent systems (Figure 1). These popu-lations are isolated by vast expanses ofopen ocean or by warm tropical watersthat restrict movement across the equa-tor. Sardines and anchovies are a peren-nial concern to marine resource managersbecause they represent the majority of theclupeoid biomass in highly productive

boundary current systems, and becauseregional populations of both groups showstrong fluctuations in abundance thathave been attributed to high levels of ex-ploitation (Murphy 1966, 1967). For ex-ample, the biomass of sardines (Sardinopscaeruleus) in the California Current peakedat an estimated 3,600,000 metric tons(MT) in the 1930s (Murphy 1966) then de-clined during a period of intensive har-vests to about 5,000–6,000 MT in 1975(Barnes et al. 1992; Wolf 1992). The bio-mass of California anchovies (Engraulismordax) has also fluctuated from lows inthe 1950s to a high in the 1970s (Lo andMethot 1989). All of the regional popula-tions of sardines and anchovies have sim-ilar histories of declines and partial recov-eries which are attributed to harvests orto climatic and oceanographic changes(Lluch-Belda et al. 1989).

Here we review genetic evidence fromallozyme and mtDNA datasets for sardinesand anchovies that may bear imprints ofpopulation collapses (bottlenecks), meta-population dynamics (extinctions and re-

colonizations), founder events, dispersals,and divergence between isolated popula-tions. These case histories are used toevaluate the hypotheses that have beenforwarded to explain shallow gene gene-alogies in other marine fishes. The forcesthat attenuate mtDNA diversity may be akey to understanding population regula-tion in marine fishes. Hence these shallowintraspecific phylogenies carry implica-tions for microevolution and marine bio-geography as well as resource manage-ment in the face of climatic change andhigh exploitation (Hansen et al. 1981; San-ter et al. 1996).

Long-Term Climatic Variability andPopulation Abundance Cycles

It is widely accepted that climatic changesare capable of limiting abundances, butthe impact of these changes on marinebiodiversity has only recently been appre-ciated (Hayward 1997; Roemmich andMcGowan 1995; Watson et al. 1996). Rapidchanges in oceanic temperature over the

Grant and Bowen • Shallow Genetic Architectures in Marine Fishes 417

Figure 2. Majority-rule bootstrap of neighbor-joiningtrees representing phylogenetic relationships amongtaxa of sardines (Sardina, and Sardinops). Percentagebootstrap (over loci for allozymes, over nucleotidesites for sequences) support indicated at nodes oftrees. (a) Nei’s unbiased genetic distances based on 34protein-coding loci (Grant and Leslie 1996). (b) Se-quence divergences based on a 220 bp sequence in thecytochrome b gene of mitochondrial DNA (Grant et al.,unpublished data).

last few tens of thousands of years, cor-responding to major climatic shifts, havebeen recorded in ice cores from Greenland(Dansgaard et al. 1993; GRIP Members1993) and Antarctica (Jouzel et al. 1993;Lorius et al. 1985). These regime shifts,some of which have occurred on a timescale of only a few decades, drastically al-tered major ocean circulation and temper-ature patterns (Lehman and Kiegwin1992). Recent decade-scale shifts in theKuroshio Current led, in part, to a rapiddecline of Japanese sardines in the 1940s(Kawasaki 1993; Kawasaki and Omori1995).

On scales of centuries and millennia,abundances of sardines and anchovies inthe California Current have fluctuatedgreatly. Based on scale deposition rates inanaerobic sediments, Baumgartner et al.(1992) identified nine population declinesand recoveries over the last 1,700 years.During this interval the estimated abun-dance of the California sardine fluctuatedfrom less than 1 million MT to at least 4million MT. These fluctuations predatefishing activity along the California coastand thus are attributable entirely to natu-ral biotic, climatic, and oceanic changes.

The earth’s climate oscillates on severaltime scales with various amplitudes. Forexample, the population fluctuations doc-umented by Baumgartner et al. (1992) forsardines occurred during a period of rel-atively minor climatic shifts. Over the pre-ceding 100,000 years, the amplitude ofglobal climatic oscillations, as recorded inGreenland ice cores, was much greater(GRIP Members 1993). These North Atlan-tic changes corresponded to temperatureand salinity shifts in many of the world’soceans (Broecker 1995). Imprints of tem-perature fluctuations in ice cores reachingback about 250,000 years also indicatestrong climatic variability (Dansgaard etal. 1993). On yet a deeper temporal scale,climates have greatly fluctuated duringthe four major Pleistocene glaciationsreaching back 1.7 million years. Thesechanges have undoubtedly led to popula-tion crashes and expansions, and possiblyto extinctions of some regional sardineand anchovy populations in the majorboundary currents of the world.

Sardines (Sardina, Sardinops)

Northwest Atlantic and Indian–Pacific sar-dines are divided into two genera. Sardinain European waters consists of a singlespecies, S. pilchardus, that extended in his-torical times from West Africa to the North

Sea in the Atlantic and from the westernMediterranean to the western margin ofthe Black Sea (Figure 1a). Sardinops inhab-its five upwelling zones of the Indian–Pa-cific Ocean characterized by high levels ofprimary and secondary productivity, in-cluding southern Africa, Australia–NewZealand, Chile–Peru, west-central NorthAmerica, and Japan. In the light of recentmolecular data, the taxonomy of these re-gional populations is uncertain, and wewill refer to them by their traditional spe-cies names: S. ocellatus (S. Africa), S. neo-pilchardus (Australia), S. sagax (Chile), S.caeruleus (California), and S. melanostictus(Japan). The geographic distributions ofthe regional populations are generallybounded by the 138C and 258C isotherms,since temperatures above 278C are lethalto adults and larvae (Parrish et al. 1989).Sardines are notably absent in the westernAtlantic, even though the temperate zonesof the northwest and southwest Atlanticappear to be suitable for sardines, andboth regions host populations of ancho-vies.

The proposal that current Indian–Pacificsardine populations are ephemeral orhave become established only recently isbased on the observation that present-daypopulations of Sardinops are shallow twigsat the termini of an ancient lineage ex-tending back to the Miocene. In an analy-sis of 34 allozyme loci, Grant and Leslie(1996) reported a Nei’s genetic distance ofD 5 1.04 (60.24 SE) (Figure 2a) betweenthe Atlantic–Mediterranean (Sardina) andIndian–Pacific (Sardinops) forms. An ap-proximate time frame for this separation

can be calibrated with divergences be-tween fish populations separated by therise of the Isthmus of Panama about 3 mil-lion years ago (Grant 1987; Keigwin 1978,1982; Vawter et al. 1980) and by dispersalthrough the Bering Strait, also about 3 mil-lions years ago, prior to the late Pliocenecooling of the Arctic Ocean (Grant 1984;Grant and Stahl 1988; Grant et al. 1984).The resulting clock (D 5 1.0 about 19 mil-lion years) yields an estimate of the diver-gence time between Sardina and Sardinopsof about 19 million years BP (15–24 millionyears). This time frame coincides closelywith the collision of the African plateagainst southern Europe (Steininger et al.1985), a vicariant event which divided theTethys Sea into Atlantic and Indian-Pacificcomponents. An alternative scenario, pos-tulated by Okazaki et al. (1996), is that theinitial split between ancestral sardine pop-ulations occurred via the Isthmus of Pan-ama. However, the magnitudes of the allo-zyme genetic distance between Sardinaand Sardinops and sequence divergencebetween cytochrome b sequences (Figure2) contradict this recent separation.

Although both allozyme and mtDNAdata point to a deep evolutionary historyfor Sardinops, divergence among present-day populations reflects only a shallowhistory reaching back less than half a mil-lion years (Bowen and Grant 1997; Grantet al., in press; Grant and Leslie 1996).This shallow time frame and the low levelsof allozyme and morphological diversityindicate that present sardine populationshave expanded only recently around therim of the Indian– Pacific Ocean. At leasttwo legacies of this colonization processare apparent in the genetic data. One is asignificant excess of low-frequency allo-zyme alleles over that expected with drift-mutation equilibrium in datasets for Indi-an–Pacific sardines (Grant and Leslie1996), for California sardines (Hedgecocket al. 1989), and for South African sardines(Grant 1985). Such an excess is usually at-tributed to the retention of new mutationsduring population growth or expansion(Watterson 1984). Another indication thatIndian–Pacific sardines have recently ex-panded is a Poisson-like distribution of thenumber of nucleotide differences ob-served in comparisons of cytochrome bsequences (Grant et al., in press). This dis-tribution is attributed in other species tomutation-drift disequilibrium caused byexplosive population growth (Rogers andHarpending 1992).

Phylogenetic relationships among re-gional populations are not resolved with


Table 1. mtDNA haplotype and nucleotide diversities and allozyme diversities in sardines (Sardina,Sardinops)

Region

Control regiona

h p n

Cytochrome bb

h p n

Allozymesc

H n

SardinaEurope 0.36 0.002 5 0.024 26

SardinopsSouth Africa 1.00 0.02 15 0.62 0.004 15 0.036 46Australia 1.00 0.02 15 0.62 0.004 15 0.045 50Chile 1.00 0.03 18 0.76 0.006 15 0.037 30California 1.00 0.03 15 0.76 0.007 15 0.036 30

0.010 149d

Japan 0.96 0.01 18 0.67 0.005 14 0.022 50

a Bowen and Grant 1997.b Grant et al., in press.c Grant and Leslie 1996.d Hedgecock et al. 1989.

the allozyme data of Grant and Leslie(1996) because of the recency of diver-gence (Figure 2a); estimates of allozymegene diversities ranged from 0.045 in Aus-tralian sardines to 0.022 in Japanese sar-dines (Table 1). Hedgecock et al. (1989)reported an estimate of H 5 0.010 for Cal-ifornia sardines and concluded that an an-cient population bottleneck or founder ef-fect may have reduced genetic diversity.These diversity values are low relative tothose reported for other marine fishes(Ward et al. 1994) and much lower thandiversities in other clupeiform fishes (seeTable 8 in Hedgecock et al. 1989). In con-trast, polymorphisms in the mtDNA con-trol region and cytochrome b are relativelyabundant, presumably due to the elevatedmutation rate in mitochondrial DNA rela-tive to nuclear protein-coding loci. ThemtDNA gene trees, consisting of a networkof minimal mutational distances betweenhaplotypes for both the control region(Bowen and Grant 1997) and cytochromeb (Grant et al., in press), indicate a prob-able dispersal pathway around the rim ofthe Indian–Pacific Ocean connecting SouthAfrica and Australia, with Chile, California,and Japan (Figure 3a,b).

Shallow divergences among these re-gional populations may be explained bytwo alternative models of population per-sistence and dispersal. First, Sardinopsmay have inhabited a limited area formost of the last 20 million years before ex-panding to the temperate corners of theIndian and Pacific Oceans in the last fewhundred thousand years. Alternatively, re-gional Sardinops populations may havebeen extinguished repeatedly and recolon-ized by transoceanic or transequatorialmigrants. Genetic analyses of present-daypopulations alone may not be able to re-solve these alternative scenarios. While

expected gene genealogical patterns arequite different under the two models, theymay have converged in present-day pop-ulations due to regional extinctions thaterased evidence of previous populationhistories (Figure 4). Fortunately, paleocli-mate and fossil records may eventually of-fer a resolution of these two scenarios. Ina study of marine Pleistocene and Plio-cene sediments from coastal California,Fitch (1969) reported a conspicuous ab-sence of sardine hard parts but a contin-uous record of other common species[hake (Merluccius), mackerel (Trachurus),and anchovy (Engraulis)]. Sardines alsowere not detected in elevated marine de-posits dating from about 100,000 to 3 mil-lions years BP, but were present in NativeAmerican middens about 7,000 years BP(Casteel 1975). Although temporal resolu-tion in elevated marine deposits is notprecise, these studies yield an approxi-mate time frame for the arrival of the pres-ent Sardinops population in the CaliforniaCurrent. It is not yet clear, however,whether this was the initial colonizationor the most recent event in an extinction/recolonization cycle; a fossil record ex-tending back 5–20 million years is neededto resolve this issue. Nonetheless, theseresults are consistent with the geneticdata in indicating that shallow gene gene-alogies in Sardinops populations are due(at least in part) to a late Pleistocene dis-persal around the rim of the Pacific Ocean.

Anchovies (Engraulis)

Anchovies are active plankton feedersfound in the same temperate boundarycurrents as sardines, but additionally oc-cur in less productive areas off Argentina–Brazil and in the western North Atlantic(Figure 1b). Regional populations of an-

chovies belong to a single genus, Engrau-lis, but the level of morphological differ-entiation between Old World and NewWorld species indicates that a separate ge-nus for Old World species may be war-ranted (Hubbs 1952; Whitehead 1973).The taxonomy of anchovies is further con-fused by the inclusion of three tropicalspecies (genus Cetengraulis) within themorphologically based phylogenetic treeof Engraulis (Nelson 1984). Molecular datareinforce the arguments for revision of an-chovy taxonomy, but we will refer to re-gional populations by traditional speciesnames: E. encrasicolus (Europe), E. capen-sis (southern Africa), E. australis (Austra-lia), E. japonicus (Japan), E. mordax(California–Mexico), E. ringens (Chile–Peru),E. anchoita (Argentina–Brazil), and E. eu-rystole (Atlantic U.S.–Canada).

Genetic partitions in anchovies aremarkedly different from those in sardines.The analyses of 31 allozyme loci (Figure5a) and 521 bp of cytochrome b (Figure5b) indicate that anchovies are dividedinto four relatively deep lineages corre-sponding to the three New World species(E. anchoita, E. ringens, E. mordax), and alineage consisting of all Old World speciescombined: E. japonicus, E. australis, E. ca-pensis, E. encrasicolus (and presumablyWest Atlantic E. eurystole, which was notassayed but which is morphologicallyvery similar to the European anchovy E.encrasicolus). Large genetic distances inthe allozyme survey and levels of mtDNAsequence divergence indicate that thefour primary lineages have been isolatedfor 6–10 million years. Shallow genetic dis-tances among the Old World species, how-ever, indicate dispersal events within thelast few hundreds of thousands of yearsand possibly more recently in some cases(Table 2, Figure 6).

While the Old World anchovies areclosely related, three of the four (except-ing the southern African population E. ca-pensis) contain high levels of intraregionalgenetic diversity relative to the shallowseparations between species. For exam-ple, two deep mtDNA lineages occur in Eu-ropean anchovies, the apparent result ofisolation between Black and Mediterra-nean Sea populations during glacial maxi-ma in the early Pleistocene (Magoulas etal. 1996). An average sequence divergenceof d 5 2.2% between haplotypes in thesetwo lineages (Grant WS and Bowen BW,unpublished data) is consistent with thistime frame. These lineages are in apparentsecondary contact and are codistributedthroughout the Mediterranean Sea and ad-


Figure 3. Parsimony network of mtDNA haplotypes in sardines (Sardina, Sardinops). (a) Cytochrome-b. Crossbars represent transitions and ovals represent transversions between haplotypes. Asterisks indicate amino acidreplacements. Haplotypes in Sardina based on a 220 bp sequence; those in Sardinops based on a 258 bp sequence(Grant et al., in press). (b) Control region. Transversion haplotypes based on a 500 bp fragment (Bowen and Grant1997).

Figure 5. Majority rule, neighbor-joining trees rep-resenting phylogenetic relationships among taxa of an-chovies (Engraulis). Percentage bootstrap support in-dicated at the nodes of trees. (a) Nei’s (1978) unbiasedgenetic distances based on 31 protein-coding loci(Grant et al., unpublished data). (b) Sequence diver-gences based on a 521 bp sequence in the cytochromeb gene of mitochondrial DNA (Grant et al., unpublisheddata).

Table 2. mtDNA haplotype and nucleotidediversities and allozyme diversities in anchovies(Engraulis)

Species

mtDNAa

h p n

Allozymesb

H n

anchoita 0.44 0.001 19 0.137 60ringens 0.41 0.001 17 0.087 30mordax 0.88 0.007 14 0.063 30

0.075 432japonicus 0.91 0.010 20 0.044 30

0.067 30c

australis 0.90 0.009 16 0.105 51capensis 0.21 0.004 18 0.091 60

0.115 3,019d

encrasicolus 0.94 0.015 16 0.060 250.88 0.016 140e 0.055 634f

0.75 0.017 749g

a 521X bp sequence of cytochrome b; from Grant WS andBowen BW, unpublished data, except where noted.

b 31 loci; from Grant WS and Leslie RW, unpublisheddata, except where noted.

c 22 loci; Fujio and Kato 1979.d 31 loci; Grant 1985.e RFLP analysis of 2.5 kb PCR fragment of ND5/6 genes

of NADH dehydrogenase complex; Bembo et al. 1995.f 24 loci; Bembo et al. 1996.g RFLP analysis of entire mtDNA molecule; Magoulas et

al. 1996.

Figure 4. Models of sardine evolution. (a) Ancientpopulation with a recent geographic expansion. (b)Population histories of extinctions and recolonizations.

jacent Atlantic Ocean. Since the averagesequence divergence between Japaneseand European haplotypes is only margin-ally larger, d 5 2.9%, the colonization ofanchovies into Mediterranean waters ap-pears to have occurred in the late Plio-cene or early Pleistocene, possibly facili-tated by a global cooling trend. Becausecontinental configurations during this in-terval were essentially the same as theyare now, and because a route of coloniza-tion across northern Eurasia was infeasi-ble due to ice accumulation, the only dis-persal pathway between Japan and Eu-rope was around the tip of southern Africaand northward to the Mediterranean (seeFigure 6). The intermediate position ofsome Australian haplotypes in the parsi-mony network is consistent with thisroute. However, the haplotypes in present-day populations of southern African an-

chovies are not intermediate between Eu-ropean and Australian anchovies, but areembedded in the network of Europeanhaplotypes. This feature of the parsimonynetwork indicates that a previous south-ern African population has become extinctand has been recolonized from Europewithin the last few tens of thousands ofyears. Notably the reintroduced anchoviesin southern Africa contain both of the Eu-ropean mtDNA lineages, implying a colo-nization event after the reassociation ofthe Black Sea and Mediterranean forms.


Figure 6. Parsimony network of 58 cytochrome b haplotypes in anchovies (Engraulis). Haplotype crossbars rep-resent nucleotide substitutions between haplotypes based on a 521 bp sequence (Grant et al., unpublished data).

A similar scenario, invoking the possi-bility of extinction and recolonization, isapparent in the relationship between Jap-anese and Australian anchovies. Whilesome of the Australian haplotypes are in-termediate between Japan and Europeanlineages, recent recurring contact betweenAustralia and Japan is also strongly impli-cated. Australian samples include repre-sentatives from at least two deep branch-es of the Japanese network, and Japanesesamples include haplotypes that are moreclosely related to endemic Australian hap-lotypes than to other Japanese haplo-types. The latter observation strongly im-plies (but does not prove) a back-dispers-al from Australia to Japan after the mostrecent colonization of Australian waters.

In contrast to the case for Old World an-chovies, genetic signatures of extinctionsand recolonization are not apparentamong the three species of New World an-chovies: E. mordax off the west coast ofNorth America, E. anchoita off Argentinaand Brazil, and E. ringens off Chile andPeru. The deep levels of mtDNA sequencedivergence between these species indicatethat regional forms have been isolated forat least 6 million years. Despite these an-cient origins, these three species also arecharacterized by low-to-moderate levels ofnucleotide diversity (Table 2) and star-shaped phylogenies consisting of a centralabundant haplotype with a few ‘‘satellite’’haplotypes distinguished by one or twomutations (especially E. anchoita and E.ringens, see Figure 6). As noted for the sar-dines, these characteristics may be evi-dence of recent expansion from a smallnumber of ancestors. Since low mtDNA di-versity within these species cannot bereadily attributed to recent colonization

or founding events, within-region popula-tion dynamics are clearly implicated, in-cluding severe population fluctuations,strong natural selection on haplotypes, orextinctions and recolonizations on a localscale (within-region metapopulation struc-ture) (see Lluch- Belda et al. 1989). Para-doxically, E. anchoita and E. ringens havethe highest allozyme heterozygositiesamong the anchovies, providing anotherreminder that population processes maydifferentially affect mtDNA and allozymediversity (Grant and Leslie 1992), and thatcaution is indicated when inferring popu-lation processes from any single class ofgenetic loci (Bernatchez and Osinov 1995;Karl and Avise 1992; Karl et al. 1992; Pal-umbi and Baker 1994).

Shallow Genetic Architectures inSardines and Anchovies

The findings outlined above lead to sev-eral conclusions about the genetic archi-tectures of clupeoid fishes inhabiting theworld’s temperate boundary currents.First, the processes shaping the geneticarchitectures of regional populations ofglobally distributed species can be under-stood only in light of metapopulation dy-namics on a planetary scale. For example,we observe low genetic diversity in mostof the surveyed sardine populations, butanalyses of within-region diversity will notreveal whether this is due to recent origin(founder event) or to large fluctuations inabundance (bottleneck). The consequencesof these two processes in terms of extantgenetic diversity can be nearly identical(Figure 4). However, a rangewide compar-ison of sister forms can distinguish be-tween these explanations. The shallow di-

vergences within Indian–Pacific popula-tions of sardines and some populations ofanchovies (especially the southern Afri-can form) are attributed to recent founderevents, because these regional types areclosely related to sister taxa. The shallowdivergences observed in Argentine–Brazil-ian and Chilean–Peruvian anchovies areattributed to within-region processes be-cause these lineages are distantly relatedto sister species (on a scale of 6–10 millionyears). Both within- and between-regioncomparisons are necessary to demon-strate that at least two processes (founderevents and bottlenecks) are responsiblefor the shallow genetic architecture of an-chovy and sardine populations.

Second, mechanisms influencing the ge-netic architectures of regional sardine andanchovy populations are probably linkedwith global trends (or oscillations) inoceanography and climate. In recent de-cades the size of regional sardine and an-chovy stocks could be estimated by themagnitudes of commercial catches and re-search surveys, and attempts were madeto correlate abundances with cyclic warm-ing events such as El Ninos (Moser et al.1987; Smith and Moser 1988). The south-ern oscillations that produce rapid and re-gionwide changes in sea surface tempera-tures and upwelling intensities will direct-ly influence zooplankton abundance in lar-val nursery areas, and hence regulate theabundances of spawning biomass. Roem-mich and McGowan (1995) and Haywardet al. (1996) note an order of magnitudereduction in zooplankton abundance inthe California Current in recent decades.Our terrestrial perspective is apparentwhen a decline in sardines during thesame period is deemed a mystery. A com-parable decline in faunal biomass of a ter-restrial ecosystem would be obvious, aswould the reason for corresponding de-clines of primary consumers. Notably thismajor decline in sardines occurred duringa relatively gentle fluctuation in compari-son to the magnitudes of climatic cyclesin the last 250,000 years (Dansgaard et al.1993; GRIP Members 1993).

Third, we observe considerable vari-ability in the magnitudes of genetic diver-gences between regional forms. On theshallowest scale, sardines and anchoviesof southern Africa share haplotypes withfish in Australia and Europe, respectively.On the deepest scale, we observe se-quence divergences of 17% between an-chovies from California–Mexico and Peru–Chile. Taken as a whole, we see a broadrange of genetic separations from the very


Table 3. Nei’s (1972, 1978) genetic distances (D) between populations (based on allozyme frequencies),geographic range of samples, and genetic distance from sister species for species of marine fishes

Species Dbetweensamples

Geographicrange

D withsisterspecies

Reference

AnglerfishLophius vomerinus 0.0007 SE Atlantic 0.45 Leslie and Grant 1990; Grant and Leslie

1993

AnchovyEngraulis spp. 0.047 Old World 0.93 Grant et al., unpublished dataE. anchoita 0.003 Argentina-Brazil 0.75 Grant et al., unpublished dataE. mordax 0.002 California 0.85 Hedgecock et al. 1989; Grant et al., un-

published data

CodGadus morhua 0.0037 North Atlantic 0.42 Grant and Stahl 1988; Mork et al. 1985G. macrocephalus 0.025 North Pacific 0.42 Grant et al. 1987b; Grant and Stahl 1988

BigeyeHeteropriacanthuscruentatus

,0.01 Central Pacific 0.69 Rosenblatt and Waples 1986

HakeMerluccius capensis 0.0006 SE Atlantic 0.23 Grant et al. 1987a; Grant, unpublished

dataM. paradoxus 0.0007 SE Atlantic 0.48 Grant et al. 1987a; Grant, unpublished

data

HalibutHippoglossus stenolepis 0.0002 NW Pacific 0.16 Grant et al. 1984H. hippoglossus 0.001 North Atlantic 0.16 Fevolden and Haug 1988; Grant et al.

1984

HerringClupea harengus 0.001 North Atlantic 0.27 Grant 1984, 1986

0.0005 Ryman et al. 1984C. pallasi 0.039a North Pacific 0.27 Grant and Utter 1984; Grant 1986

MilkfishChanos chanos 0.002 Central Pacific .1.0b Winans 1980

MulletMugil cephalus 0.03 Central Pacific 0.62 Rosenblatt and Waples 1986

SardineSardinops sagax 0.005 Indian-Pacific 1.04 Grant and Leslie 1996

PufferfishSpotted green puffer

Arothron hispidus ,0.01 Central Pacific 0.56 Rosenblatt and Waples 1986Guinaefowl puffer

A. meleagris 0.03 Central Pacific 0.56 Rosenblatt and Waples 1986

a Average distance between major east-west subdivision in North Pacific. Nei’s distance within each group averages0.0004.

b Monotypic genus; sister taxon uncertain.

young to the very old, probably reflectingthe diversity of outcomes that can affectspecies in fluctuating habitats.

Finally, we observed some discordancebetween the levels of diversity in nuclearand mitochondrial assays: Indian–Pacificsardines had high haplotype diversity butlow allozyme diversity, while two NewWorld anchovies had low haplotype diver-sities but high allozyme diversities. Sex-specific differences in dispersal or strong-ly skewed sex ratios can explain such dis-parities in other species, but there is noevidence that these factors operate in clu-peoid fishes. A more likely explanation in-vokes the relative rate of evolution andthe inheritance dynamics of mitochondrial

versus protein-coding nuclear loci. Duringpopulation declines, the loss of genetic di-versity will be accelerated in mtDNA rela-tive to nuclear DNA due to the lower ef-fective population size of this maternallyinherited genome. During population growththe mitochondrial genome will accumulatemutations more rapidly than protein-cod-ing nuclear loci due to a higher rate of se-quence evolution. Hence allozyme diver-sity might be higher shortly after popula-tion crashes and mtDNA diversity mightbe higher during a recovery phase withhigh levels of population growth. Giventhe climate-associated processes outlinedabove, we may expect to see both condi-tions in sardines and anchovies. In the

next section we explore the general signif-icance of shallow genealogies for under-standing the evolution and population bi-ology of marine fishes.

Inferences About PopulationHistory From Genetic Diversity

Shallow genetic separations within spe-cies, relative to large divergence betweensister species, are characteristic of manymarine fishes that have been examinedwith allozymes and mtDNA sequences.Two results are notable in allozyme sur-veys (Table 3). One is that sister speciesof many marine fishes have been isolatedfor a few to several million years, basedon genetic distances calibrated with well-dated geologic events. Second, the level ofdifferentiation between populations withinmany species is an order of magnitudeless than the level between sister species.In these cases, the similarity of allele fre-quencies between populations may be at-tributed to mixing of eggs, larvae, andadults on extended temporal and spatialscales (Waples 1987). However, surveys ofmicrosatellite DNA, which has a muchhigher mutation rate, may reveal mixingon time scales of decades and centuries(Bentzen et al. 1996).

The analysis of mtDNA sequences al-lows marine fishes (Table 4) to be cate-gorized into four classifications (Table 5)based on different combinations of smalland large values for haplotype diversity(h, a measure of the frequencies and num-bers of haplotypes among individuals,varying between 0–1.0) and nucleotide di-versity (p, average weighted sequence di-vergence between haplotypes, varying be-tween 0 for no divergence to over 10% forvery deep divergences). Ideally, compari-sons of gene genealogies between speciesshould be made with homologous seg-ments of DNA, but the scientific literatureon marine fishes is not yet rich enough toallow a review based on a single segment.Table 4 contains examples from restrictionfragment analyses of the whole mtDNAmolecule as well as direct sequencing ofparticular mtDNA genes (cytochrome b,ND4/5, and cytochrome oxidase). Muta-tion rates are certain to vary somewhatamong these different sequence assays(see Irwin et al. 1991; Saccone et al. 1987;Walker et al. 1995), but are probably notradically different for RFLP and mitochon-drial coding regions (Birt et al. 1995; Lambet al. 1994). Direct comparisons amongthe different mtDNA assays are justifiedhere because the focus is on the pattern


Table 4. Haplotype and nucleotide diversities, geographic range of samples, and percentage sequence divergence from sister taxon for species of marinefishes

Species Haplotypediversity(h)

Nucleotidediversity(p %)

Geographicrange

Sequencedivergencefrom sisterspecies (%)

Reference

Category 1Cod, Atlantic 0.30 0.13c North Atlantic Carr et al. 1995

0.36 0.18 NW Atlantic Carr and Marshall 1991; Zwanenburget al. 1992

0.30 NW Atlantic Pepin and Carr 1993Beaugregory damselfish 0.41a,b 0.30 Caribbean Shulman and Bermingham 1995Bluefish 0.11 0.07 Australia Graves et al. 1992aHoki 0.28 0.08 SW Pacific, SE Atlantic Baker et al. 1995Red snapper 0.13a 0.13 Gulf of Mexico Camper et al. 1993Red grouper 0.42a 0.08 Gulf of Mexico Richardson and Gold 1993Weakfish 0.13 0.13 NW Atlantic Graves et al. 1992b

Category 2Blue marlin 0.84a 0.54 Atlantic–Indo-Pacific Graves and McDowell 1995

0.74 0.33 Atlantic 3.5 Finnerty and Block 19920.60 0.16 Pacific 3.5 Finnerty and Block 1992

Sailfish 0.80a 0.32 Atlantic–Indo-Pacific 3.5 Graves and McDowell 1995; Finnerty andBlock 1992

White/striped marlin 0.82 0.29 Pacific Graves and McDowell 1995Atlantic–Pacific 3.9 Finnerty and Block 1992

Shortfin mako 0.76a 0.35 Worldwide Heist et al. 1996Orange roughy 0.37a 0.19 SW Pacific, SE Atlantic Smolenski et al. 1993

0.74 0.59 SW Pacific, SE Atlantic Baker et al. 1995French grunt 0.78a,b 0.62 Caribbean Shulman and Bermingham 1995Goldspost goby 0.98a,b 0.68 Caribbean Shulman and Bermingham 1995Longjaw squirrelfish 0.94a,b 0.62 Caribbean Shulman and Bermingham 1995Slippery dick 0.78a,b 0.62 Caribbean Shulman and Bermingham 1995Sergeant major 0.79a,b 0.49 Caribbean 4.50 Shulman and Bermingham 1995

Bermingham et al. 1997Bluehead 0.55a,b 0.48 Caribbean Shulman and Bermingham 1995Greater amberjack 0.90 0.34 Gulf of Mexico Richardson and Gold 1993Haddock 0.87 0.59 NW Atlantic Zwanenburg et al. 1992Cape hake 0.90a 0.57 SE Atlantic Becker et al. 1988Deepwater hake 0.68a 0.55 SE Atlantic Becker et al. 1988Capelin 0.81a 0.42 NW Atlantic 3.42a Dodson et al. 1991

0.98a 0.51 NE Atlantic 3.42a Dodson et al. 1991Atlantic herring 0.91a 0.55 NW Atlantic Kornfield and Bogdanowicz 1987Pacific herring 0.90a 0.49 NE Pacific Schweigert and Withler 1990Spanish sardine 0.83 0.53 W Atlantic Tringali and Wilson 1993Red Drum 0.95a 0.58 Gulf of Mexico Gold et al. 1993

0.90a 0.56 NW Atlantic Gold et al. 1993Stickleback 0.93 0.71 N Atlantic–Pacific Orti et al. 1994

Category 4Bluefish 0.70 1.23 NW Atlantic Graves et al. 1992aAtlantic menhaden 1.00a 3.20 NW Atlantic Bowen and Avise 1990Gulf menhaden 1.00a 1.00 Gulf of Mexico Bowen and Avise 1990Redlip blenny 1.00a,b 1.09 Caribbean 12.4 Shulman and Bermingham 1995; Berming-

ham et al. 1997

a Based on restriction enzyme analysis of whole mtDNA.b Average within population h.c Average percentage sequence divergence among haplotypes.

of genetic diversity rather than the abso-lute magnitudes.

The first category includes species withsmall values of both (h , 0.5 and p ,0.5%). One example is the anchovy ofsouthern Africa (h 5 0.21, p 5 0.40%),which, as we have shown, may representa recent recolonization from Europe. An-

other example is Atlantic cod (h 5 0.32, p5 0.15%), which show little genetic diver-gence across the North Atlantic (Mork etal. 1985). Since ongoing gene flow betweenthe northeast and northwest Atlantic isunlikely based on distribution and life his-tory, the lack of differentiation (in con-junction with biogeographic evidence)

points to a regional extinction duringPleistocene glaciation, followed by a post-glacial range expansion (Carr et al. 1995;Pogson et al. 1995). While such founderevents are probably an important factor,these events cannot explain all the speciesin category one. Anchovies off Chile– Peru(h 5 0.41, p 5 0.10%) and off Argentina–


Table 5. Interpreting haplotype and nucleotidediversities for marine fishes

p

h

Small Large

Small 1. Recent populationbottleneck orfounder event bysingle or a fewmtDNA lineages.

2. Population bottle-neck followed by rap-id population growthand accumulation ofmutations.

Large 3. Divergence be-tween geographi-cally subdividedpopulations.

4. Large stable popula-tion with long evolu-tionary history orsecondary contactbetween differentiat-ed lineages.

Brazil (h 5 0.44, p 5 0.10%) also have lowhaplotype and nucleotide diversities, butthe ancient origin of these forms pre-cludes an explanation based on recent col-onization. Other mechanisms such as pe-riodic regionwide bottlenecks or metapop-ulation structure within regions must beinvoked to produce the observed low lev-els of diversity. Other examples in cate-gory 1 include Beaugregory damselfish (h5 0.41, p 5 0.30%), Australian bluefish (h5 0.11, p 5 0.07%), hoki (h 5 0.28, p 50.08%), red snapper (h 5 0.13, p 5 0.13%),and weakfish (h 5 0.13, p 5 0.13%). Al-though little is known about the evolution-ary histories of these fishes, their geneticarchitectures uniformly indicate periodsof low effective population size within re-cent thousands or tens of thousands ofyears.

The second category consists of popu-lations with high h and low p. This con-dition is attributed to expansion after aperiod of low effective population size;rapid population growth enhances the re-tention of new mutations (Avise et al.1984; Rogers and Harpending 1987). Ex-amples are typically drawn from large pop-ulations or entire species which containone or two prevalent haplotypes embed-ded in a cluster of ‘‘twigs’’ that are one ora few mutations removed from the centralhaplotypes. This second category in-cludes several of the billfishes (h 5 0.68–0.85, p 5 0.29–0.54%), shortfin mako (h 50.76, p 5 0.35%), as well as northwest At-lantic capelin, northeast Atlantic capelin,goldspot goby, French grunt, slipperydick, longjaw squirrelfish, greater amber-jack, haddock, Cape hake, northwest At-lantic and northeast Pacific herring, reddrum, and west Atlantic Spanish sardine(h 5 0.79–0.98, p 5 0.29–0.68%). Many ofthese species are believed to have origi-nated in the Pliocene or early Pleistocene,but their mtDNA genealogies coalesce on

a more recent scale, perhaps the last fewhundred thousand years.

A third category, low h and high p, char-acterizes populations with a few highly di-vergent haplotypes. This condition mayresult from secondary contact betweenisolated populations or by a strong bottle-neck in a formerly large, stable population.Secondary reassociation of formerly iso-lated populations is certain to occur in themarine realm (see Veron 1995), and retic-ulation of isolated lineages may be rela-tively common, but this must be coupledwith low effective population sizes (tomaintain low h) in order to fit the criteriaof category 3. Coastal and oceanic fishesare usually not subdivided into small iso-lated populations, so it may be that fewopen-ocean fish fit into this category. Suchconditions may be more applicable to in-shore fauna (Burton 1986; Planes and Do-herty 1997) and freshwater organisms(Bermingham and Avise 1986).

The fourth category consists of specieswith large values of both h and p. The highlevel of divergence between haplotypesmay be attributed to secondary contactbetween previously differentiated allopat-ric lineages (as in category 3) or to a longevolutionary history in a large stable pop-ulation. Examples of the first conditionmay include the European anchovy (h 50.86, p 5 1.6%) and Atlantic menhaden (h5 1.0, p 5 3.20%), both of which containa pair of divergent and twiggy mtDNA lin-eages which (based on geographic consid-erations) probably arose in isolation. Pos-sible examples of the second condition in-clude the Japanese anchovy (h 5 0.91, p5 1.0%), Atlantic bluefish (h 5 0.70, p 51.23%), Caribbean blenny (h 5 1.0, p 51.09%), and Gulf menhaden (h 5 1.0, p 51.0%), for which extended geographic iso-lation is unlikely because of the configu-ration of the open coastline where theyoccur (Japanese anchovy and Gulf men-haden) or because of strong dispersal ca-pabilities (bluefish). It is notable that evenin category 4 the levels of divergences be-tween lineages are typically an order ofmagnitude less than the divergence be-tween sister taxa.

Shallow Genetic Architectures inMarine Fishes

These four categories are defined by de-mographic events that alter the likelihoodof mtDNA lineage survival and the time toancestral coalescence of lineages. Most ofthe species in Table 4 fit the first or sec-ond categories, which include populations

with a recent coalescence of mtDNA lin-eages and shallow histories. It is clear thatshifts in climate or oceanographic condi-tions can be responsible for this condi-tion. What additional factors contribute tothis trend? Using recursive simulations,Avise et al. (1984) showed that in a stablepopulation there is a high probability thatall haplotypes in the population can betraced to a single female after 4N genera-tions, where N is the female effective pop-ulation size. Hence the loss of female lin-eages will accelerate in declining popula-tions or during fluctuations in abundance,and the expected time to coalescence ofextant lineages will be correspondinglyshorter. A second factor known to pro-duce shallow coalescence of extant lin-eages is a large variance in reproductivesuccess, which can decrease the geneticeffective size of a population without ac-tually reducing population size (Hedge-cock 1994; Hedgecock et al. 1994). Marinefishes tend to have very large reproduc-tive potentials (although exceptions exist,especially among the cartilaginous fishes),but propitious combinations of biologicaland physical conditions are required forlarvae to survive and recruit into the adultpopulation. Under conditions of high vari-ance in reproductive success, an entireyear class may be the product of relativelyfew matings. Evidence for such sweep-stakes recruitment in marine fishes comesfrom the observation of genetic differ-ences among individual schools of Califor-nia anchovies (Hedgecock 1994), BlackSea anchovies (Altukhov 1990), south Af-rican anchovies (Grant 1985), Norwegiansprat (Sprattus sprattus; Nævdal 1968), andredfish (Sebastes mentella; Altukhov 1990).In these cases the effective populationsize for maternally inherited genes may beone or two orders of magnitude smallerthan the census size (see Bowen and Avise1990), leading to higher rates of lineage ex-tinction than in populations of the samesize with many successful spawners.

On the other hand, life-history patternsproducing strong population subdivisionsmay increase the time to coalescence, butnumerous allozyme studies indicate thatmarine fishes do not have strong popula-tion partitions relative to freshwater andanadromous fishes (see Ward et al. 1994).Lower levels of differentiation betweenmarine fish populations are attributed tohigher dispersal potential during plank-tonic egg, larval, or adult life-historystages, coupled with an absence of physi-cal barriers to movement between oceanbasins or adjacent continental margins. In


contrast, strong population subdivisions(and corresponding barriers) for freshwa-ter fishes may serve to retain divergentlineages (see Bermingham and Avise 1986;Mayden 1993). The physical factors whichbuffer freshwater fish lineages against ex-tinctions are notably absent from the ma-rine realm.

Conclusion—ConservationLessons

Marine fishes are generally regarded as re-sistant to extinction because of large dif-fuse populations and because marine wa-ters are often viewed as boundless habi-tats. As a result, few species of marine fishare considered to be strong conservationconcerns (Vincent and Hall 1996). How-ever, several factors promoting lineageturnover and shallow population structurein several time scales may make marinefishes vulnerable to overharvesting andclimate change. Lineage sorting fromsweepstakes recruitment takes place on ascale of generations and is proportional tothe magnitude of the reproductive vari-ance in the population. Major populationfluctuations, at least in sardines and an-chovies, take place on a scale of decadesand centuries. Regional extinctions, dis-persal events, and recolonizations takeplace on a scale of thousands to millionsof years. The relative importance of thesefactors may differ between tropical andtemperate zones, and between specieswith diverse life histories. Nonetheless,they probably all contribute to the ob-served trend of shallow genetic architec-ture in marine fishes.

What are the implications of shallowmtDNA population structure and low ge-netic diversity for the conservation of ma-rine fishes? First, it is apparent that this isa widespread phenomenon among marinefishes, and therefore only exacerbated inrecent decades by deteriorating coastaland pelagic habitats (Sherman 1994) andfishing activities. If natural conditionscommonly result in low mtDNA diversityin marine fishes, then such findings do notinvariably signal inbreeding depression orother genetic health problems. However,evolutionarily rapid drops in genetic di-versity due to fishing (Smith et al. 1991),and the loss of low-frequency alleles (notusually detected by estimates of hetero-zygosity) may be of special concern to thegenetic health of marine species and tothe maintenance of their evolutionary po-tential (Ryman et al. 1991).

Second, even very large populations can

be susceptible to regional extinction. Thepassenger pigeon analogy may be appro-priate for coastal marine fishes, especiallythose in upwelling zones and other fluc-tuating but productive habitats. Most ofthe demographic indices of healthy ma-rine fish populations are ratcheted down-ward by overharvesting, and in manycases the majority of the biomass in heavi-ly fished populations consists of youngfish. Under these circumstances, recruit-ment failures over 3 or 4 years could leadnot only to commercial extinction but tothe total extinction of a regional popula-tion or species. At least for sardines andanchovies, genetic imprints indicate thatregional collapses occur without the add-ed burden of intense harvesting. There-fore, management strategies for sardineand anchovy fisheries, which are amongthe most productive harvests on the plan-et, must include allowances for the fragil-ity of populations in unstable habitats. De-pleted stocks will not invariably recover.

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