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Defining EvolutionarilySignificant Unitsfor conservation

Craig MoritzCraig Moritz is at th e Dept of Zoology an dCentre for Conservation Biology,The Un iversity of Queenslan d,Qld 4072,Australia.

writing in the first issue of TREE,Ryder brought the term Evolution-arily Significant U nit (ESU) to the atten-tion of a broad audience of ecologists andevolutionary biologists. The E SU conceptwas developed to provide a rational basis

for prioritizing taxa for conservationeffort (e.g. captive breeding), given thatresources are limited and that existingtaxonomy may not adequately reflectunderlying genetic diversity*. With theexplicit recognition of the genetic com-ponent of biodiversity in conservationlegislation of many coun tries and in theConvention on Biological Diversity, theESU concept is set to become increas-ingly significant for conservation of naturalas well as captive populations.However, the ESU remains poorly de-fined, both conceptually and operation-ally. Most definitions suggest than an ESUshould be geographically discrete, bu tgenetic criteria range from significant di-vergence of allele frequencies3 throughsome level of genetic distance to congru-ently structured phylogenies amo nggene+. Several authors have arguedthat an ESU should display concordantdivergence for both mo lecular and non-molecular traitG6. Althoug h all are try-ing to achieve the sam e end, it seemsthat the operational definitions varyaccording to the biological and legislat-ive context. The purpose of this essay isto revisit the ESU concept in relation torecent developm ents in molecular p opu-lation genetics. The suggested defi-nitions and criteria are not suppo sed tobe proscriptive - rather, the intention isto promote debate on the purpose andpractice of using genetic information todefine conservation units.Conservation goals: what do wemean by significant?The overriding purpose of definingESUs is to ensure tha t evolutionary heri-tage is recognized and protected andthat the evolutionary potential inh erentacross the set of ESU s is maintaine d. Fora given set of populations we cannot pre-diet future outcom es, but we can make

inferences abo ut the evolutionary past.Thus, the term significant in ESU shouldbe seen a s a recognition that the set ofpopulations has been historically iso-lated and , accordingly, is likely to have adistinct potential. According to thisview, the empha sis is on historical popu-lation structure rather than currentadaptation. This departs from the moreusual concern that we should seek tomaintain the full array of differentlyadapted geographic variants within aspecies3J. I suggest that to focus onmaintain ing the full array of locallyadapted variants is not only difficult inpractice, but also negates the evol-utionary process that we seek to main-tain, insofar as preservation of variantsadapted to previous conditions may re-tard the response to natural selection.There may, of course, be other non-evolutionary reasons (e.g. ecological,economic, aesthetic) for ascribingconservation value to a particular popu-lation.The recognition of ESU s is primarilyrelevant to long-term management issues,that is, defining conservation prioritiesand setting strategy, although in the shortterm it may be prudent to avoid trans-locating individuals between ESUS,~.Criteria for recognizing an ESUDefining an ESU as a historically iso-lated set of populations leads to a quali-tative criterion based on the distributionof alleles in relation to their phylogeny(Fig. 1). Simulation stud ies suggest thatit takes abou t 4 N generations from thetime that two popu lations separate forthere to be a high probability of theirhaving reciprocally m onophyletic allelesg.Because of its relatively low effectivepopulation size and high substitution rate,animal m itochondrial DNA (mtDNA) isexpected to achieve this condition morerapidly than nuclear alleles. Indeed, well-differentiated sister species may havereciprocally monop hyletic mtD NA butphylogenetically unsorted alleles at nu-clear loci (e.g. northern versus southernelephant sealslo). To require reciprocalmonophyly for both nuclear and mtDNAgenes (as required for genealogicalconcordance4) seems overly restrictive.Nonetheless, significant divergence innuclear allele frequencies should be re-quired to avoid misclassifying populationslinked by nuclear, but not organellar, geneflow.

100

P 50

0-0 200 400 600 800

Generations1whWy II paraphyly

ab cd abc d a bedA-E-

__ - - -A BA 0

Ill reciprocal monophyly

ab cd-T B

Fig. 1. Development of phylogenetlc structur-mg of alleles between populations. The graph(modifiedrom Ref. 8) shows the results of 100simulations with two daughter populationsfounded with 20 and 30 lndlviduals and allowedto grow rapidly to N = 200. P indicates the prob-ability of alleles (a-d) within the two populations(A, 6) being (I) polyphyletic. (II) paraphyletic or(Ill) reciprocally monophyletlc. After the divisionof one populatton Into two, the phylogeneticrelations of the alleles in the two daughterpopulations typlcally proceed from polyphyly,through various paraphyletlc conditions to re-clprocal monophyly as ancestral polymorphismsare sorted and replaced by derived statesg.The rate depends on effective population size,usually taking at least 4N generations toachieve reciprocal monophyly, and is also influ-enced by mutation rate. population demographyand the phylogeographlc dlstributlon of allelesbefore the separation of the two populations.

The above theory sugge sts a geneticcriterion for recognizing a n ESU : ESCsshould be reciprocally monophyletic formtDN A alleles and show significant diver-gence of allele frequ encies at nuclear locr.Although such a definition may seemto be overly restrictive in some cases (seebelow), it has the advan tages of beingtheoretically sound and of avoiding theissue of how much divergence is enough?that plagues quantitative criteria such asallele frequency divergence and geneticdistance. It considers the pattern ratherthan the extent of sequence divergence,as it is not the intention to ascribe con-servation value to an ESU in relation tomtDNA distance.

Contrast with management unitsand stocksIn practice, genetic analyses oftenreveal differences between sampledpopulations ranging from reciprocal mon-

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ophyly, through substan tial b ut incom-plete phylogenetic separation, to minorbut statistically significant differences inallele frequency. Populations that do notshow reciprocal m onophyly for mtD NAalleles, yet have diverged in allele fre-quency, are significant for conservationin that they represent populations con-nected by such low levels of gene flowthat they are functionally independent.The recognition of such M anagementUnits (MUs) is fundamental to propershort-term man agem ent of the more in-clusive ESU s, in that MU s are the logicalunit for population monitoring and demo-graphic study.MlJs are therefore recognized as popu-lations with significant dive%ence of allelefrequencies at nuclear or mitochondrialloci, regardless of the phylogenetic distinc-tiveness of the alleles. The distinction be-tween ESUs and MU s is important, as itaffects ways in which genetic evidenceis obtained and interpreted.To use genetic information effectively,we should therefore distinguish b etweentwo types of conservation units, both im-portant for management: ESUs,concernedwith historical popu lation structure,mtDNA phylogeny and long-term con-servation needs; and M Us, addressingcurrent po pulation structure, allele fre-quencies and short-term managementissues. The concept of discrete stocksas used for marine speciessJ2 sometimes

comb ines the two types of unit. Dizonet al.5 attempted to clarify the definitionof stocks using a hierarchy of phylogeo-graphic pattern in conjunction with otherevidence. Although their scheme wasexplicit, it remained unwieldy and didnot recognize the different conservationgoals. I sugge st that the term stock be re-stricted to short-term man ageme nt issues(e.g. mon itoring h arvests, etc.) and, in re-lation to genetics, be treated as synony-mous with MU s as defined above.Application and limitationsThe foregoing treatment was writ-ten with animal populations undergoingpredominantly divergent evolution inmind. In practice, ESU s will usually ca mplement rather th an replace species de-fined under traditional, predom inantlymorphological criteria (although ESUsand species would be synonymous undersome species conceptslJ4). Given theshortage of resources for man aging majorecosystems, let alone previously d e-scribed species, it is logical to focus gen -etic studies on species of greatest con-cern. How ever, an exciting extension is toapply these principles to whole communi-ties - using comparative phylogeographyto define geographic areas where com-ponent species have evolutionary histor-ies separate from their conspecific+.This could have considerable significancefor planning of regional reserve systems.

The iden tification of ESU s as definedabove requires information on the distri-bution and phylogeny of mtDN A allelesand on the distribution of nuclear alleles.In contrast, only information on allelefrequency is directly pertinent to the de-lineation of MU s, although for smallsamples and loci with high substitutionrates, sequence information may providemore power for detecting populationsubdivisioni6. T hese types of data areaccum ulating rapidly for threatened orexploited species 11J5,17.or green turtles(Chelonia mydas), the genetic data suggesttwo ESU s - one in the Atlantic Ocean andthe other in the lndoPacific - each con-sisting of numerous MU s (Fig. 2). Here,the black turtle (C m. agassizi) representsjust one M U within the larger lndo -PacificESU. The hum pback whale (Megapteranovaengliae), another intensively stud-ied species, app ears to represent a singleESU with num erous MU s, many of whichcorrespond to major stocks recognizedfrom migration routes18.As with any evolutionary property ofpopulations or species, the definition ofthe ESU needs to be applied with com-mon sense. In some circumstances it mayseem overly restrictive. For example,where there has been rapid speciationor recent hybridization, mtD NA allelesmay not yet be sorted between other-wise discrete taxa. However, the failureto define these as separate ESU s should

Indo-Pacific, \

Hawaii (16) hi-Hawai i (6)

Galapagos (8)Mexico (7)Oman(15) I

Atlantic-Mediterranean @I.

Aves (1)Costa Rica (15)Florida (,21)

F lor ida , (3)Cyprus (10)Aves (7)Sur iname (15)Ascens ion (1)Ascens ion (34)Brazil (15)

0 0.8 0 0.6% Sequence d ivergence

Brazil (1)Guinea B iaaau (1 2)

F l o r i d aCosta RicaVenezuela

S u r i n a m eA s c e n s i o n

Braz i lA f r ica

C y p r u sO m a nAust ra l iaJapanHawaii

Mexico-B~~apacJ~

FlA C6R VEN SUR ASC BRA AFR CYP OMA AUS JAP HAW MEX-B GAL

0 P>O.O50 m Po and anonym ous s ing le copy nuc lear sequence+. A major phy logeograp hic breakis ev ident between mtDNAs f rom At lant ic -Medi ter ranean and Indo-Pac i f ic rooker ies (a), suppo r ted by s l ight , but s ign i f icant var ia t ion in nuc lear genes. St ructur ing o fa l le le f requenc ies among rooker ies wi th in e i ther area was substant ia l for mtDNA and less marked, but s t i l l s ign i f icant for the nuc lear loc i (b) . Accord ing ly , the spec iesshou ld be managed as two ESUs (At lant ic -Medi ter ranean and Indo-Pac i f ic ) each cons is t ing o f mul t ip le MUs. Reanalys is o f mtDNAs by sequenc in g o f cont ro l reg ionsequences can great ly in crease th e reso lu t ion o f MUs (e .g . f rom 3 to 9 in the Aust ra las ian reg ion22) but has not a l tered the percept io n o f ESUs.

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not affect conservation priorities be -cause the taxa in question are probablyalready recognized as species on broaderbiological criteria. A group of popu lations,such as North Atlantic humpback whales,which shows substantial but incompletephylogenetic sorting of mtD NA allelesr8,would not be classified as a separate ESU ,but still warran t conservation attention asseparate management units. Conversely,the criteria may be oversensitive in somecases in species of very low vagility wheremost local popu lations are strongly dif-ferentiated for mtD NA and nuclear genes(e.g. Ensatir~G). In this circumstance,the genetic differences need to be inter-preted in the context of the total vari-ation within the species. An additionalcaveat is that the identification of ESU sand MU s is susceptible to error becauseof insufficient sampling: the analysis oftoo few individuals or populations couldlead to the false recognition of ES& .;samp ling too few nucleotides or too fewnuclear loci could lead to failure to rec-ognize important genetic patterns.Future directionsThe concepts and criteria for ESU san dMU s expounded above seem logical andtheoretically valid, but it remains to beseen whether they are practical. Pertinentdata are expanding rapidly. but there is

a need for further theoretical study of thedynam ics of allele distribution and phy-logeny in demo graphic contexts relevantto threatened and exploited species. Thisis certainly a field where close interactionbetween experim ental and theoreticalbiologists would pay off.AcknowledgementsThanks to John Avise, Brian Bowen,Peter D wyer, Peter Hale, Shane Lave ry,Nancy Fitzsimmons and Steve Palumbifor critical reviews of the manuscript, toAnita Heideman and Lyn Pryor forpreparation of figures and to theinmates of the Conservation Geneticslab for inspiration. Supported bygrants from the Australian ResearchCouncil.References

Ryder, O.A. 1986)Trends Ecol. Euol. 1,9-10Avise, J.C. (1989) Trends Ecol. Em/. 4,279-281Waples. R.S. (1991) Mar. Fish. Reu 53,1 -22Avise, .C. and Ball, R.M. (1990) Oxf Suru. Euol.Biol. 7,45-68Dizon, A.E.. Lockyer, C ., Perrin, W.F.,Demaster, D.P. and Sisson. J. (1992) Cons.BioL6.24-36Vogler, A.P., Knisley, C .B., Glueck, S.B..Hill, J.M. and DeSalle, R. (1993) Mel Ecol 2.375-384

The early evolution of life:solution to Darwins dilemma

J . Wi l l i am Schop fWilliam Schopf is at the Dept of Earth &Space Sciences, Center for the Study ofEvolution and the Origin of Life, instituteof Geophysics and Planetary P hysics,

and Molecular Biology Institute,University of California,Los Angeles, CA 90024, USA.

In 1859, Charles Darwin stated theproblem:If the theory [of evolution] be true it isindisputable that before the lowestCambrian stratum was deposited longperiods elapsed . and that during thesevast periods the world swarmed with liv-ing creatures . . [However], to the ques-tion why we do not find rich fossilifer-

ous deposits belonging to these earliestperiods . I can give no satisfactoryanswer. The case at present must remaininexplicable . ..* (Ref. 1, Ch. X)

Surprisingly, it was not until morethan a century later, with publication ofthree pivotal papers in 1965 2-4and of amajor m onograph in 19685, that searchfor the m issing Precamb rian fossil rec-ord was demo nstrated to be a fruitfularea of scientific inquiry. Since that time -in a scant three decades - m ore than 3000taxonomic occu rrences of microscopicfossils have been discovered in nearly400 Precamb rian geological formations6.7;the new field of Precam brian paleobi-ology has emerged, matured and becomeestablished worldw ide as a viable sub-discipline of the natural science+; andmost recently, two mammoth compendia,prepared by international groups of re-spected ex perts, have summ arized thestatus of this interdisciplinary area ofscience,. To a major extent, Darwins di-lemma has been resolved - much of themissing fossil record has been uncovered.What has been learned? Where does thisyoung field go from here?

As in any emerging area of science,numerous new generalizations have beendrawn, four of which stand out as beingparticularly significant.(1) Life originated very early in Earth his-tory, much earlier than had been assumed.Before the discovery of the Precamb rianfossil record, few imagine d that the welldocum ented history of Phanerozoic life -the familiar progression from seaweedsto flowering plants, from trilobites tohum ans -wa s merely the tip of the evol-utionary iceberg. Indeed, the recent dis-covery of diverse cellularly preservedmicroorganisms in the 3465 t 5-million-year-old Apex chert of Western A ustraliaindicates that the Phanerozoic temporallyencom passed less than 15% of all of evol-ution, and that living systems have existedfor more than three-quarters of the historyof the plan et (F ig. 1). Moreover, becausemost of the 1 1 species described fromthis earliest known fossiliferous depositare comp arable to extant (oscillatori-acean) cyanobacteria - oxygen-producingphotoautotroph s that are amon g themost highly evolved of all eubacteria- it seems certain that life mu st haveoriginated substan tially (an d probablyhund reds of millions of years) earlier.

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Ryman. N. C 991) F&h Em/ 39 (SuppI. A21 -224Avise. J.C. (1994) Molecular Murken.Xatural Histoy and Eoolutron. Chapman &HallNeigel. J. and Avise. J.C. (1986) inEuolutionuy Processes and Theory (Nevo, 1..and Karlin, S.. rds). pp. 515-53 4. AcademicPressSlade. R.W..Moritz. C. and Heideman. A.(1994) hlol. Brol. Ecol 11,341-X6Moritz. C. (1994 ) ,bfo/ Era/. 3.403-413Gauldie, R.W. (1991) Gun. ! F& 7 Aquat. Sri. 48,722-731Cracraft, J. (1983) Cinr Omitho/. 1.159-187Frost, D.R.and Hillis, D.M. (1990)Herpetologrca 46. 87-104Avise, J.C. (1992) Olkos 63. 62-76Hudson, R.R.. Boos. D.D .and Kaplan, N.L.(1992) Mol. Rio/. Euol 9, 138-151Hoelzel. A.R., ed. (1991) Genetics andConsrm ution of Whales and Dolphins.International Whaling CommissionBaker, C.S.et al ( 1993) Proc. /Vat/ Acad. SciUSA 90, 8239-8243Moritz. C.. Schneider. C.J. and W ake. D.B.(1992) syst Biol 41. 73-291Bowen. B.W.etal (1!)92)Evolution 46,865-881Karl, S.A.. Bowen. B.W. and A vise. J.C. (1992)Genetics 131. 163-173Norman, J.. M oritz. C. and Limpus. C.J. (1994)Mol. Ecol 3. 3Kb-37:i

What has been learned?