This article was downloaded by:[De Queiroz, Kevin] [Smithsonian Institution Libraries] On: 16 November 2007 Access Details: [subscription number 777121151] Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Systematic Publication details, including instructions for authors and subscription information: http://www.informaworld.com/smpp/title~content=t713658732 Concepts and Species Delimitation Kevin De Queiroz a a Department of , National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

First Published on: 01 December 2007 To cite this Article: De Queiroz, Kevin (2007) 'Species Concepts and Species Delimitation', Systematic Biology, 56:6, 879 - 886 To link to this article: DOI: 10.1080/10635150701701083 URL: http://dx.doi.org/10.1080/10635150701701083

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf This article maybe used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November 2007 O:10.1080/10635150701701083 DOI: online 1076-836X / print 1063-5157 ISSN: Copyright Biol. Syst. s o odtrietebudre n ubr of numbers and boundaries delimitation—that data. the species emperical from determine of species to issue species—is how the the is, to of concept tied theoretical closely disagree- the current conclusions about is, ments different problem—that concept to species these lead the incom- Thus, species. can of of numbers are and they boundaries Many the concerning definitions that wording). associated in given of patible their any details and that minor concepts that so definitions in a with concept, associated differ is be a may definition concept of species a even description (where are concise there definitions and alternative concepts, more species 24 listed named (1997) Mayden different 1998). incom- de Harrison, 1997; 1998; partially Mayden, Queiroz, by least (reviewed biol- at concepts of species and patible subgroups different different advocate currently ogists The that itself. species is of concept problem the confused involving problem been a has by delimitation species of issue the tury, delimitation. species to of devoted symposia topic have the biologists organ- why and cells is for which do isms, they species as entire them, at perceive looking to by simply humans for impossible more it less makes or This ephemeral. their are organisms) among (i.e., connections parts the Moreover, hu- their observers. than also man lived longer species and larger them, much observing generally are orga- humans of the 2005a). level than higher Queiroz, a nization orga- de at exist also biological species see because of However, 1982; levels Mayr, the (e.g., lower of nization at some organisms, units and fundamental cells, in fun- genes, comparable the to them of making importance one biology, are of units species damental authors, various to cording r mne fteiprac fseisi ilg.Ac- biology. in species of importance the of eminded To edr of Readers opiaemtes o ogl h athl cen- half past the roughly for matters, complicate 66:7–8,2007 56(6):879–886,  c eeo e ehd fseisdlmtto htaentte otoepoete.[pce ocp;seisciei;species criteria; species concept; [Species properties. those to to biologists most tied encouraging perhaps not more criteria, are and though species that Fourth, species, traditional delimitation corroboration. delimitation.] the a species of from of of degree away existence methods higher emphasis new the a shifts develop with for concept associated the evidence secondary species are Third, is unified as evidence separation. interpreted) relevant a lineage of treated significantly, appropriately of lines considered formerly (if evidence more properties longer properties provide thus they the the and no that properties of of extent are one the all any criteria to conceptualization Second, of delimitation species species delimitation. species presence to secondary of species species relevant to issues former are of criteria only the the concept species as but First, unified separated; criteria conceptualization following: This clearly species species the separation. are secondary to including lineage delimitation former delimitation, assessing the species species to and and for relevant species consequences criteria) of several (operational property has evidence necessary of only lines the separately a different as as secondary existence treating lineage as by achieved monophyly) metapopulation diagnosability, be can acquired isolation, concept evolving properties metapopulation species reproductive different unified intrinsic evolving A adopting criteria). (e.g., in separately species divergence (secondary disagree a properties of they defining as course but category, the existence species boundaries during treating the the lineages of in inferring by property agree for defining methods concepts primary and the species category as Alternative species lineage the species. of of definition numbers the and both concerning controversy of century half Abstract.— oit fSseai Biologists Systematic of Society ytmtcBiology Systematic eateto etbaeZooy ainlMsu fNtrlHsoy mtsna nttto,Washington, Institution, Smithsonian History, Natural of Museum National Zoology, Vertebrate of Department h su fseisdlmtto a ogbe ofsdwt hto pce ocpulzto,laigt a to leading conceptualization, species of that with confused been long has delimitation species of issue The pce ocpsadSeisDelimitation Species and Concepts Species adyne obe to need hardly C25006,UA -al [email protected] E-mail: USA; 20560-0162, DC K VNDE EVIN 879 Q fauie pce ocp o h rbe fspecies of problem consequences the for the concept of delimitation. species some unified examine a then of will 2005b, 2005a, I 1999, 2005c). 1998, pub- Queiroz, have (de I the previously di- which unified, lished how review be about can will proposal concepts species a moreverse I and a paper, problem ap- concept in this to species delimitation In biologists species way. allows of straightforward it uni- problem that a the is of proach benefits concept significant species most species fied the the of of con- definition the One the also category. thus about and debates species of endless cept seemingly our- a free from As to position species. selves a of in now concept are unified biologists consequence, a for basis the provides which unity, defini- conceptual underlying and an exhibit they concepts tions, species among alternative differences obvious contemporary the Despite appears. it as ous foeo h lentv pce ocps uha the as such concepts, species adoption alternative than the taxa of species one fewer of of recognition leads the concept species to biological the of adoption ex- which situations For in to attention incompatible. called have partially authors of several least ample, many at advocates are addition, concepts have In the concepts biologists. these contemporary of among all Importantly, ers. oth- among proposed concepts, ecologi- phylogenetic and biological, these evolutionary, likely cal, familiar of are the include some journal which this least concepts, of at readers about Most knowledgeable based. which are the upon properties they the with of terms biologists, con- in defined contemporary species categories by alternative advocated of categories cepts major of consists UEIROZ otntl,ti pce ocp rbe snta seri- as not is problem concept species this Fortunately, T be1i ito lentv pce ocps h list The concepts. species alternative of list a is 1 able A LTERNATIVE S PECIES C ONCEPTS Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November 2007 uio,19,fra lentv emnlg) l fteeiescnomt igegnrlcnetudrwihseisaeeutdwith equated are species which of under (lines criteria concept operational for general as proposal de interpreted single the (see appropriately a concepts more under to are species that separation. (*) distinct conform lineage Note properties diverging considered ideas assessing the (*). be by to these of asterisk longer relevant crossed many of no evidence) an and thresholds would All with lineages, represent table terminology). metapopulation marked this that evolving alternative are in separately properties) an species summarized of ideas for of various converses properties 1998, the the necessary Queiroz, paper, (or as this in Properties viewed described commonly 2005). unification are Queiroz, that de and from lineages (modified based are they hntc*omapeei lse qatttv ifrne ihnr(90;SkladCoel 17) Sneath (1970); Crovello and Sokal (1970); Michener difference) (quantitative cluster phenetic a *Form genetic entries) of four (deficits next cluster (see genotypic a *Form (definition) cluster Genotypic Advocates/references Phenetic entries) four next demographic (see or Heterogeneous (genetic cohesion Phenotypic and tendencies, role, evolutionary Unique of components (all zone adaptive or niche *Same Phylogenetic Cohesion Property(ies) Evolutionary in resulting reproduction (natural Ecological Interbreeding Biological concept Species biol- for hand, other the geneticists On population systematists. for molecular key and are ones genetic whereas taxonomists, museum and paleontologists for central are differences morphological Similarly, systematists. for fundamen- tal are study monophyly and who diagnosability ecolo- and biologists for gists, paramount to are differences importance niche zones, central hybrid of incompatibili- are reproductive ties example, For subgroups biologists. different to of interest greatest of various differ- are the phyloge- because properties expected, these the be Moreover, to are of emphasis 1). in version (Table ences diagnosable concept the species of netic case differences the state character in ecologi- fixed a the and of of concept, case species the occupation cal in zone concept, adaptive species or niche biological distinct the of sion intrinsic example, r for based; are concepts of alternative several the which upon properties biological different the Zink, 1983; Cracraft, 1979; 1996). Wanntorp, and concept Bremer species (e.g., phylogenetic the of version diagnosable 880 poutv slto ntecs fteioainver- isolation the of case the in isolation eproductive igoal Dansblt qaiaie xddfeec)Nlo n ltik(91;Carf 18) Nixon (1983); Cracraft (1981); Platnick and Nelson difference) fixed (qualitative, *Diagnosability Willmann and Meier (1989); Ridley (1966); a Hennig of alleles (all alleles of coalescence *Exclusive of all and ancestor an of splits (consisting lineage *Monophyly when extinct Diagnosable becomes Ancestor 2001) (1999, Grismer Genealogical Monophyletic difference) fixed (qualitative, *Diagnosability Hennigian fertilization interpretations) or (some recognition mate specific *Shared of (absence isolation reproductive *Intrinsic Recognition Isolation h esnfrteeicmaiiiishst owith do to has incompatibilities these for reason The T ABLE .Atraiecneprr pce ocps(.. ao lse fcneprr pce entos n h rprisuo which upon properties the and definitions) species contemporary of classes major (i.e., concepts species contemporary Alternative 1. nemdae;eg,heterozygotes) e.g., intermediates; other of those species) with shared not common allele a ancestral from descended are gene given states) character derived shared of possession from inferred commonly descendants; its exchangeability) fate historical interact) organisms conspecific which with environment the fertilization) and mating for one another recognize gametes, their or organisms, conspecific which by (mechanisms system barriers) to [geographic] opposed extrinsic as properties, intrinsic on based organisms heterospecific between interbreeding offspring) fertile and viable SYSTEMATIC BI oemrt.Te r l ae nipratbiological important have on to based properties. seem all are concepts They the merits. of some all investments interests, personal research own their and from back those step or can approach, who multidisciplinary a adopt who ogists n eaouainlnae,o oeseicly with evolv- specifically, more separately or with lineages, species metapopulation equates ing refer concept in I general way which The the to conceptualized. to are fundamental species is impor-which element equally shared and, that element tant, species common contemporary a all share out, concepts turns it As concepts. empha- among rival similarities, by the than solution rather the differences, the obscure sizing to problem instead concept species tended the have solve species. to of attempts concept Previous general, more single, a implies element, which common a identifying is concepts alter- species the native reconciling to key the 2005c), 2005b, 2005a, 1999, sIhv rudpeiul eg,d uio,1998, Queiroz, de (e.g., previously argued have I As LG VOL. OLOGY alt(1995) Mallet Ball and Avise also see (1995); Shaw and Baum (1985) Mishler (1985); Donoghue (1979); Rosen T (1997) Mayden (1978); Wiley (1951); Simpson Va and Lambert (1987); al. et Masters (1985); Paterson (1970) Dobzhansky (1942); Mayr W mltn(99 1998a) (1989, empleton ih 14) ar(92;Dbhnk (1950) Dobzhansky (1942); Mayr (1940); right (1990) (1995) Spencer n oa (1973) Sokal and (1990) Wheeler and (2000) nV h omnElement Common The R ln(96;Adrsn(1990) Andersson (1976); alen ECONCILIATION 56 Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November 2007 fmn emnsta aeu uhaseislevel species a such up make that lineage. one form- segments here but thereby is many point species species, given of The other Any lineages. lineage. to level) rise a (species ing give such species of that lineage segment is metapopulation Fi- a entire groups. only an family not but and is species demes of a population- as end nally, the lower such the of continuum, at end the populations higher from the continuum, used at level is con- reside traditionally It to are sidered which 2004). species, Gaggiotti, distinguish to and here subpopulations Hanski connected 1970; of (Levins, up (separate made lineages population mono- several sive term or of The up a made branches). lineage generally with a is confused called also but be sometimes is to which group, not phyletic simply is or It metapopulations 1951). of case this a in 1980) Hull, r term the here clarify, To lineages. such of segments 2007 ocpulzdi em fafwgnrlevolutionary general few a em- of been terms have in to be conceptualized that can sense phenomena biologists). general contemporary by the a phasized in of the used all during (here encompass times speciation different at of arise process they that species is incompatible concepts to lead criteria) species (secondary so forth. and subpopulations, (mono- its or of organisms, terms concept genes, in component monophyletic be species has also phylogenetic it version), phyly the under phenetic distinguish- phenetically able; the be under to has niche; also it different concept, a species lineage occupy the to concept, has species lin- also ecological other the from to under has isolated eages; also reproductively lineage intrinsically the concept, be species evolving biological separately version the isolation a of the is under but species lineage, a metapopulation under concepts, al- Thus, species the properties. all of defining of secondary most properties as different that lineages adopt is concepts of point species been The properties ternative have category. defining 1) species Table secondary the in as of asterisk treated many an implicitly that with positing marked concepts species by (those alternative underlie for con- that accounted properties species the of be diversity can the cepts then category, of property species defining the primary the separately the consider be are to we element species If common that lineages). com- idea metapopulation the the evolving of (i.e., context element the among mon in differences concepts the species consider alternative we Clarifica- when agreement. conceptual emerges general tion exist this how can of consider concepts spite to species in instructive about disagreement is much it so 1998), Queiroz, sepa- evidence, de of) (for see (segments lineages are metapopulation species evolving rately that view common the fr oa netrdsedn eis(ipo,1961; (Simpson, series ancestor-descendant an to efers eaouainetne hog ie(f Simpson, (cf. time through extended metapopulation h esnta hs ifrn eodr properties secondary different these that reason The share concepts species contemporary all that Given h Differences The metapopulation EQ DE ERZSEISCNET N PCE DELIMITATION SPECIES AND CONCEPTS UEIROZ—SPECIES r fr oa inclu- an to efers lineage rusi em fmlil eetes hsi as fthe of cause is This trees. per- gene multiple yet, of terms later in groups (monophyletic) cutoff exclusive form the lineages draw both where will haps perhaps others later, still And somewhat rier. bar- reproductive cutoff intrinsic an develop the lineages the where distinguishable. draw phenetically will lineages Others char- the quantitative diver- make in of acters differences process the where will in perhaps people early gence, some lin- relatively Thus, cutoff evolving species. the separately a draw become a have considering to for eage cutoff lines) sev- horizontal its a of the as by adopts each (represented concepts that property species different is contemporary reason different The eral disagreement. there however, be between, everyone In property, will two. species, last are there single the that of a agree prop- will acquisition is first the there the after that of and agree acquisition will the everyone Before erty, gray species. the of of num- ber the side about agreement either unanimous be On will there zone, conflict. into species alternative come which concepts properties within zone of gray set large This a forms forth. so and distinct, ecologically when diagnosable, example, r distinguishable, other—for lines phenetically become each numbered they to the relative and properties from time, different more through r daugh- and another the more represent one becoming gray (i.e., lineages of divergence ter shades and separation The lineage speciation). of process the species. as rec- ognized be to different deserve lineages to which concerning lead conclusions nonetheless can that element, common reason fundamental a the sharing despite is concepts, species This different category. the species (necessary) the defining a of a adopts property as set concepts this species from is property different different problem several a of is this each reason that regular The a 1998). in Queiroz, occur (de necessarily order even not same the do at they The occur and all genes. time, not do component changes these their that of is problem terms in stages phyletic mono- and And paraphyletic, polyphyletic, ecologies. through pass distinctive they evolve They as another mates. one potential recognize longer no point organisms the the to where diverge systems recognition mate Their ible. incompat- become systems genitalia, developmental Their and states. gametes, character fixed of terms in nosable organisms) diag- component become They their distinguishable. phenetically become (or the of as they number Thus, diverge, a lineages. lineages of diverging acquisition by properties the different to in changes lead that characters is these point important the problem, species concept the to regard With behavior. and physiology, ogy, morphol- development, organis- , of including biology, aspects mal different many involve may neutral; they and or disadvantageous, quantitative; advantageous, or qualitative selectively phenotypic; may or They genotypic diverse. be highly are however, processes, by affected those characters The drift. genetic the and thereof), (or lack migration selection, natural mutation, processes: peettetmsa hc hyaqiedifferent incompatible, reproductively acquire monophyletic, eciprocally they which at times the epresent iue1i ihysmlfiddarmrepresenting diagram simplified highly a is 1 Figure 881 Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November 2007 rlntr fspecies. gen- of the nature about eral agreement species the widespread of despite exis- definitions category the incompatible for many reason so of the tence is This problem. concept species 882 rista neleterovosdfeecs nsot it short, In prop- differences. r obvious the their of underlie importance that erties the rival denying those between without conflicts con- concepts the species eliminates contemporary it all and to cepts, el- common in the is retains shift that It ement conceptualized. fundamental are still species that yet way the minor relatively in- solution a The volves problem. concept species the to solution s sterctfsfrcnieigasprtl vliglnaet have to lineage species. evolving separately a a become criteria—that considering species for cutoffs their their as as lines) is, proper- horizontal is different the reason adopt by The (represented concepts ties disagreement. species be are contemporary there will different that there after that agree however, and will between, species, everyone In first property, single last two. the a the of is of acquisition there acquisition the that the Before agree species. will of everyone property, agree- number unanimous be the will about there zone, ment gray into the come properties of concepts side of either species On alternative conflict. set which within entire zone gray The a etc.). forms they distinct, which ecologically reproductively at dis- incompatible, monophyletic, phenetically times reciprocally become the they diagnosable, represent when tinguishable, 9 (i.e., to properties 1 different acquire criterion) la- lines (species horizontal the SC the represent and beled gray time, of through shades diverging form lineages in to daughter gradations splitting The (species) (species). lineage lineages single two sim- a highly represents This 2005a). diagram 1999, plified 1998, Queiroz, de (after concepts species (1 vs. 2species) peet nfidseisconcept. species unified a epresents h iuto aejs ecie ugssasimple a suggests described just have I situation The F Gray Zone IGUR 1 Species 2 Species E .Lnaesprto n iegne(pcain and (speciation) divergence and separation Lineage 1. A nfidSeisConcept Species Unified SYSTEMATIC BI SC1 SC2 SC3 SC4 SC5 SC6 SC7 SC8 SC9 nocmn Bti 97 eursseista exhibit re- that of species study requires a 1987) partic- example, (Butlin addressing For inforcement to questions. relevant biological are ular that species those composed are of they that in important are category the species of Subcategories etc.). species, re- monophyletic (e.g., species, interest differentiated ecologically of species, properties isolated ad- productively the using describe be concept that species can jectives unified terminology the useful under more more developed therefore etc.)—a and species precise phylogenetic species, species, biological ecological (e.g., and alterna- general adjectives overly the misleading using therefore under that is, named way those concepts—that been species the that tive have to properties species contrast of the in classes on However, different possess. based recognize species species to of is, subcategories define category—that classes to species used the be can of they that is portant species in of properties issue the the delimitation. to relevant Thus, directly remain species. question different the lin- for of evidence evolving is existence separation con- separately lineage of are of) evidence eages, species (segments from as Because lineage diverge ceptualized divergence. of and evidence and provide that separate separation therefore properties and they all another as one are forth, acquire so lineages repro- and postzygotic isolation, and ductive pre- distinguishabil- monophyly, phenetic reciprocal as ity, evidence such of attributes lines properties, or criteria r operational important serve as they First, species ways. two in secondary important criteria—remain former con- it properties—the species have that Those rival the that cepts. is under properties important unified various considered the been considered embrace aforemen- be to the continues reason can from the resulting proposal of concept tioned part species important the an that species, of properties 1998). Queiroz, de question ter- is (see revised in needed a it ideas is and minology concepts, the then species to different accepted, as refer 1) is (Table to proposal appropriate longer this from no separately If evolving lineages. be to other have only considered They be species. to else anything or divergent, ecologically lineages words, isolated, diagnos- reproductively intrinsically distinguishable, other monophyletic, phenetically able, be In to existence. have during not their acquire do not of may course or the may species that properties: properties contingent considered are cate- they species Instead, gory. the of longer properties (necessary) no defining as being species—the reinterpreted concepts—are of species native properties alter- among incompatibilities necessary the created that properties as treated previously have been that properties other the all words, other this (or, the treats it as lineages Second, property thereof). metapopulation segments species properly, evolving of more concept separately general as element—the common the lvn oassigtesprto flnae.These lineages. of separation the assessing to elevant A necessary are properties certain that denying Despite retains it First, components. two has solution The LG VOL. OLOGY eodwyi hc hs rprisrmi im- remain properties these which in way second only eesr rpryo pce.In species. of property necessary 56 Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November 2007 h xsec fmtpplto iegs(e Pigliucci, 2005c). Queiroz, (see de lineages 2003; for metapopulation responsible of be existence to the hypothesized are that though phenomena definition, species his r the to finally, cohesion relevant as And identified mechanisms species. (1989) Templeton a that considered properties be to sufficiently is divergent lineage opera- a when an deciding not for is criterion tional and 2000) Willmann, and Meier of 1966:64; (Hennig, model interests hierarchical rise nested, the a give to in conformity they strict adopted when species—was species descendant ancestral to of gen- extinction the property— the distinctive to Its similar concept. species is biological eral species Hennig’s of dis- criteria. are characterization operational views (1966) by alternative the primarily of tinguished many that and species of concept general common a these represent that characterizations both More- recognized 1999). has 1999) 1998, (1997, the Mayden Queiroz, over, to (de closely concept correspond species unified thus include not and do criteria (1978) Wiley operational and 1961) (1951, Simpson of definitions species isola- the Similarly, 2005a). reproductive Queiroz, (de intrinsic tion with of incorporates criterion confused which operational definition, be the species not popular should repro-Mayr’s that sexually to organisms) theoretical restricted general ducing (though a species to of initially, concept least con- at species “biological referred, the cept” and 1970) 1969, 1950) Mayr, Dobzhansky, (e.g., 1942; later Mayr, Mayr concept” 1940; that Wright, “interbreeding-population (e.g., ideas the the termed Thus, (1963) concept. species to closely unified correspond the category species is the charac- it of proposed such, terizations previously As several application. that empirical surprising its not for used are that evidence) theoretical of (lines metapopula- criteria the operational evolving from of lineages) separately tion (as separation species clear con- of the species concept new simply a but not is cept described just concept species of properties necessary not as would properties just species. those it consid- of been authors; any have previous treat that by properties important the ered of all continue embrace would concept to species unified a that is point case, the any In in- better monophyly. exhibit be make that species might using to served phylogeny historical species-level about a ferences a uses whereas that study incompatibilities, reproductive postmating 2007 eciei h eane fti paper. this of remainder briefly will the I in which describe of some delimitation, species of issue iiainb lal eaaigtecneta problem de- conceptual species the of separating issue clearly the by clarifies limitation it that is concept species ltdt eea prtoa pce rtra represent criteria, species operational several to elated ti prpit opitothr htteunified the that here out point to appropriate is It n ftems motn osqecso unified a of consequences important most the of One A nfidseiscnethscneune o the for consequences has concept species unified C NEUNE FOR ONSEQUENCES ocpulzto essDelimitation versus Conceptualization S EQ DE PECIES ERZSEISCNET N PCE DELIMITATION SPECIES AND CONCEPTS UEIROZ—SPECIES D ELIMI TATION ul enaotda eodr pce rtra(those criteria species previ- secondary have as that adopted properties been ously the Considering numbers and species. boundaries of separa- the inferring lineage to of relevant is evidence tion concept, provides species that unified property a any of context the con- In species of delimitation. alternative issue the to the relevant considered be under should cepts emphasized properties the most the considered be to others was important. the property bat- of which ongoing over an expense in tle the engaged biologists at with 1995), properties (Bush, various the one of only emphasized each unduly which concept species in alternative situation This undesirable concept. the created alternative practice each under con- necessary was properties sidered these of one different proper- a species, necessary of as ties acquired viewed alternative were properties lineages the various diverging by which of in most concepts, issue Under species the delimitation. to relevant species are of properties different many that esetvs n ae ficmlt ieg separation. lineage incomplete of retrospective cases versus and perspectives, prospective decades etc.), versus centuries, (years versus scale relevance temporal the data, meth- separation), particular lineage of particular of inferring of for more reliability (i.e., the ods or issues: one following concerning the differences or dis- from agreements result should disagree- delimitation Instead, species category. about about species ments disagreements the of from definition purely the result that species of numbers and boundaries the about disagreements longer any no be should there species, and Thus, of concept delimitation. unified boundaries a species under is, the species—that inferring of numbers of to problem relevant conceptual) evidence than (rather of methodological different fundamentally problem lines more the are conceptual as they the viewed Instead, category. appropriately with species do the proper- defining to of those nothing issue that have revealing the ties by clarifies necessary delimitation situation considered species This of longer species. no of are properties question in erties concept. species the species about delim- disagree- ments of by species confused that of hopelessly with and issue conceptualization intertwined the intimately words, was other itation they In species. necessary, of numbers be and boundaries the to about disagreed commonly properties authors different different because considered Moreover, con- species). be a to enough sidered diverged had for lineage (i.e., a species when a deciding as considered regarded be to also lineage a were for infer necessary numbers to used and were boundaries that properties species con- same the commonly that were delimita- in issues fused (species two these species Previously of tion). the numbers inferring of and problem boundaries methodological conceptualiza- the (species from category tion) species the defining of ncnrs,udrauie pce ocp,ms of most concept, species unified a under contrast, In is concept species unified a of consequence Another ncnrs,udrauie pce ocp,teprop- the concept, species unified a under contrast, In eeac fDvreProperties Diverse of Relevance 883 Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November 2007 h bec faypstv vdnefrisexistence. its for evidence positive in any inappropriate with- of is absence go species the to a seem recognizing would that it saying out hand, other the On negative is evidence. this even popula- but of species, sets different represent more) tions (or two that absence hypothesis the the against only question, in of properties the only consid- When ering species. separate of hypothesis the against evidence constitute evidence the but constitutes separation, properties the those divergence. question: of of in one properties stages the early pro- by evidence the be vided the concerning in might exists still as asymmetry an properties, is Thus, the simply it lineage evolved if the have expected that yet is lin- not course, other may all of from prop- reason, separately those The evolving of eages. is more it or if one even lack erties might lineage a other words, In separation. lineage of hypothesis does a contradicting question in properties the hypothesis. that of supporting presence fallible) the that only but a species) a (i.e., sepa- lineage a of rate represents set property a that that that possessing guarantees not property populations is single a point of the presence the Thus, lineage. sin- a metapopulation form question gle in such populations from the inferred though be other even might data In species 2002). more Irwin, or (e.g., two words, populations of between sets regularly same exchanged the paternally being and dis- are autosomal dispersal genes when inherited low even recipro- from females of result of pattern also tances a can the in then monophyly as DNA, cal inherited, mitochondrial maternally of is case locus 1997). the Wollenberg, if and Avise However, 1994; Moritz, popu- (e.g., of lations sets distributed parapatrically or allopartically from inferred commonly r is species the separate of example, mis- existence For in- be inappropriately. are can interpreted properties evidence if the of leading line that any say contrary, to the on not fallible; is This species. a existence the of for evidence considered such be provides may property it relevant evidence, popu- single of a set a even (by of in- possession lations) Mayden, the to (compare that extent species sufficient the To separate 1999). is of separation existence the lineage fer of evidence that is any One consequences. additional has separation eage the delimitation. to species evidence) of of problem lines (as relevant of are all properties Thus, those separation. lineage of evidence distinguishabil- provides phenetic ity), fertiliza- niches, (incompatible different systems, converse tion its prop- or genetic the intermediates), of either deficits diagnosability, monophyly, 1), coalescence, isolation, Table exclusive reproductive (intrinsic in itself asterisk erty an with marked 884 cpoa oohl fteallsa ie ou in locus given a at alleles the of monophyly eciprocal igepoet osiue vdne(hc salways is (which evidence constitutes property single nteohrhn,teasneo n n rmr of more or one any of absence the hand, other the On V all eigtepoete nqeto seiec flin- of evidence as question in properties the iewing ftoepoete hudb osdrdevidence considered be should properties those of uniyo Evidence of Quantity absence against ftesm rprydoes property same the of ieg eaainta is, separation—that lineage not osiueevidence constitute presence for SYSTEMATIC BI lineage fany of not ifrn u eetysprtdseis(eQerzand Queiroz (de species separated recently but different from populations between than species widespread cally geographi- exist and to old same differences the larger within geographic populations for between exhibit possible is species it all and variation, nearly because than information crucial information Geographic is geographic approaches. of traditional use under direct more make and (Knowles consideration 2007). Carstens, under the populations within of monophyly exhibits sets question loci when sampled in even the methods separation of lineage the none for fact, evidence In provide focus. can the mono- not methods, is coalescent-based phyly new these of in case However, the concept. species phylogenetic mono- of so-called assess versions the genealogical to and used monophyletic commonly under sort phyly same is the that is information which methods of trees, These gene 2007). from information Carstens, the- use and coalescent Knowles of context (e.g., the ory delimi- in species developed for being methods tation tra- new progress. consider the example, significant on For represents based criteria longer species no of ditional hypotheses are test that to separation methods context, lineage new this In of divergence. development of the sep- stages early lineage the detecting in for aration useful these very of not most are Moreover, properties divergence. con- of the in process many cutoffs tinuous separation, artificial lineage somewhat represent of them issue of the cer- to are relevant like tainly the and monophyly, diag- (reciprocal) isolation, nosability, reproductive Although intrinsic delimitation. as species such properties for methods de- new at- and criteria velop their species shift traditional the to from away biologists tention encourages of it properties lineages, contingent those over lineages evolving arately a fot yefcieyakn epet hoeapreferred criterion. a operational choose (single) to people asking effectively by these against efforts worked has using concepts ex- species the been rival of Nonetheless, istence have years. for people evidence of some lines point multiple and This obvious, species. different seem of may existence separation, the lineage of thus of and hypotheses proper- corroborated more in several highly divergence—result lineage of during arise lines possession that multiple the ties case, is, any evidence—that to In be of separation. should of it evidence evidence difficult more find find the the in to divergence, are of be lineages another,process earlier should one the Conversely, it to separation. easier of relative the acquired therefore have and to of expected can process they be the differences of in number the are larger the lineages divergence, of along In farther existence evidence. the of the lines general, of multiple requires (i.e., species) separation separate hy- lineage corroborated highly of a pothesis separation, lineage for dence nfidseiscneti ht yepaiigsep- emphasizing by that, is concept species unified te e ehd eeatt pce delimitation species to relevant methods new Other adopting of consequences important most the Among lhuhpeec fasnl rprypoie evi- provides property single a of presence Although LG VOL. OLOGY lentvst h rdtoa Properties Traditional the to Alternatives 56 Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November 2007 steifrneo eaaeyeovn lineages. evolving separately of delimitation inference species the of as problem the more of a treatment toward explicit criteria species movement traditional represent the them from of away some that but out methods point existing to or only new review to not 2004). this is 2003, purpose Marshall, to My and contributors Sites by other reviews also by (see described issue be will several these which delimitation, about species of more to say approaches not new will other I or 2005). Miller, Manni 2004; least 2003; al., al., at et et of Manel (e.g., indicative separation are lineage partial (genetic that by characters defined phenotypic) surfaces or in to designed tra- changes are abrupt on instead identify based but not criteria are operational that ditional proposed been information recently geographic have incorporate species that methods More- involving 2007). over, Apodaca, problems and to Rissler 2007; Raxworthy, application (see its and ogy technol- system information geographic rapid of and information. recent development the with geographic change to likely incorporate is situation This explicitly 1) not (Table criteria do species traditional the of most In addition, underused. are methods anal- such in- clade 1998b), (Templeton, nested exceptions, ysis and 1979) certain (Sokal, tests with Oden, Mantel 1979), cluding and an Sokal Sokal, is 1969; 1978b; Sokal, delimitation 1978a, and species Gabriel to) (e.g., related idea old (or of methods in isolation and clines as such distance. phenomena by of species result within the occurs as that differentiation sep- lineage from (i.e., aration) discontinuities true neces- distinguish is information to taxa, Geographic sary papers.) understudied cited from the in samples as of screen- numbers when large approximations be ing first still obtaining may for methods (Such useful 2005). muta- (e.g., Vogler, 0.95 of and to equal Cardoso number or than the greater probability a estimate with correctly tions arbitrary longer more no a on parsimony will which based beyond threshold or the as 2006), such al., criterion, et Pons previously (e.g., els from particular derived Lef´ a (e.g., cases whether criterion studied divergence, operational an of meth- as level all adopt question that into calls ods situation This 1997). Good, 2007 e ocp fseisrpeet nedt seemingly to end an represents uni- a species This for and of separated. basis concept conceptual clearly fied the which are as issues under serves methodological concept theme species common unified a on The ations acceptance. widespread with and r interfered thorough has 1) more Table (see their it has perpetuate that to terminology helped misleading species the which and by concept recognized criteria are operational general the the with of species of confusion long-standing how- authors; a other ever, these by of proposed been Several have delimitation. conclusions species consequences of its problem of the some for and species of concept unified aiainta l oenseiscnet r vari- are concepts species modern all that ealization lhuhtedrc s fgorpi information geographic of use direct the Although yga nti otiuinhsbe odsrb a describe to been has contribution this in goal My C br ta. 06,tertclmod- theoretical 2006), al., et ebure ONC LUSION EQ DE ERZSEISCNET N PCE DELIMITATION SPECIES AND CONCEPTS UEIROZ—SPECIES d neprclapplications. empirical in meth- ods delimitation species different by infor- provided the mation integrating for also thus and separately lineages) constitute evolving populations of sets eval- whether for the uating for methods as to (i.e., context delimitation methods species diverse of unified problem of a relevance the provides understanding species it the Moreover, of definition category. the about debates interminable rse,L .19.A vltoaycasfiaino etlson of classification evolutionary to approach An statistical 1999. new L. A 1969. L. Sokal. Grismer, R. R. and R., K. Gabriel, and concept species biological the of critique A 1985. J. M. Donoghue, Columbia process. evolutionary the of Genetics 1970. T. Dobzhansky, Am. . their biology: and populations in Mendelian clustering 1950. T. Phenetic Dobzhansky, 1997. Good. A. D. and K., Queiroz, resolution. de their and problems species Different 2005c. K. Queiroz, de consequences its and species of concept unified species. A of 2005b. K. concept Queiroz, de modern the and Mayr Ernst 2005a. K. Queiroz, de the and species of concept lineage general The 1999. K. Queiroz, de cri- species species, of concept lineage general Or- The Curr. 1998. K. analysis. Queiroz, de speciation and concepts Species 1983. J. Cracraft, and phylogeny taxonomy, DNA 10:38. 2005. Vogler. Evol. P. Ecol. Trends A. Bush. and L. G. A., from Cardoso, Reply 1995. L. G. Bush, bio- or populations Geographic 1979. Wanntorp. H.-E. and K., Bremer, the on perspectives Genealogical 1995. Shaw. L. K. and A., D. Baum, A ecology. and A concepts Species force: driving The 1990. L. Andersson, nseiscnet sed uio,19,19,20a 05,2005c). 2005b, 2005a, 1999, 1998, Queiroz, de (see views concepts my of the species development provided on acknowledged the reviewer previously to colleagues have anonymous numerous I of an version. contributions and earlier coalescent Wiens, an on on J. comments Sites, based J. Knowles methods L. and about paper. theory, this information contribute valuable to me provided inviting for and delimitation ie .C,adK olneg 97 hlgntc n h rgnof origin the and 1997. Wollenberg. K. and C., J. vise, concor- genealogical of Principles 1990. Jr. Ball, M. R. and C., J. vise, sad nteGl fClfri,Mxc.Hreooia55:446– Herpetologica Mexico. California, of Gulf 469. the in islands 18:259–278. Zool. Syst. analysis. variation geographic 181. r York. New Press, University 84:401–418. Nat. A 27:1263–1269. BioEssays 56:196–215. Sci. Acad. Calif. Proc. taxonomy. of future the for 102:6600–6607. USA Sci. Acad. Natl. Proc. Cam- Press, MIT ed.). Wilson, Massachusetts. A. bridge, (R. 49–89 essays Pages category. interdisciplinary species New the eds.). of Berlocher, properties defining H. S. and York. Howard, New J. Press, University (D. and Oxford speciation unification conceptual and 57–75 A Species Pages speciation: recommendations. of process terminological the and teria, 1:159–187. nithol. 14:3531–3546. Ecol. Mol. the Cicindelidae). (Coleoptera: of diversification Pleistocene 28:220–224. Zool. Syst. reconstruction. phylogeny in species logical Louis. Stephenson, St. G. Garden, A. Botanical and Missouri Hoch, eds.). C. (P. biosystematics plant to proaches 289–303 Pages problem. species 94:7748–7755. USA Sci. Acad. Natl. Proc. species. Evol. Surv. Oxf. taxonomy. 7:45–67. biological Biol. and concepts species in dance T I cmedtosfrapyoeei lentv.Bylgs 88:172– Bryologist alternative. phylogenetic a for ecommendations xn39:375–382. axon hn .Wesfrognzn h 06SBsmoimo species on symposium SSB 2006 the organizing for Wiens J. thank rtqe .Rv il 72:3–30. Biol. Rev. Q. critique. A CK NOWLEDGMENTS R EFERENCES in xeietladmlclrap- molecular and Experimental iidl hybrida Cicindela in nls forms: Endless pce group species in Species: 885 Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November 2007 oiz .19.Dfiig’vltoaiysgicn nt’frconser- for units’ significant ’evolutionarily Defining 1994. C. Moritz, phylo- and developmental, morphological, The 1985. D. B. the Mishler, for software Computer (AIS): space in Alleles Biol. 2005. P. Evol. M. . Miller, to approaches Diverse 1970. D. C. Michener, Pages concept. species Hennigian The 2000. Willmann. R. and R., Meier, evolution, Diversity, thought: biological of growth of The 1982. Press E. Belknap Mayr, evolution. and species, Populations, New 1970. McGraw-Hill, E. zoology. Mayr, systematic of Principles 1969. E. Mayr, Harvard of Press Belknap evolution. and species Animal 1963. E. Mayr, Univer- Columbia species. of origin the and Systematics 1942. E. Mayr, concepts: species of hierarchy a and Consilience 1999. L. R. Mayden, adn .L 97 irrh fseiscnet:Tedenouement The concepts: species of W. hierarchy A J. 1997. Nails, L. R. D. Mayden, Potts, D. A. McKay, J. I. Rayner, J. R. C., J. Masters, Land- Gu´ 2003. E. F., Taberlet. Manni, P. and Luikart, G. Schwartz, K. Trends M. synthesis. S., modern Manel, the for definition species A 1995. J. Mallet, 77–107 Pages Extinction. 1970. R. Levins, Lef´ recog- the and Speciation 1995. without (eds.) Spencer G. species H. and Delimiting M., D. 2007. Lambert, Carstens. C. B. and L., L. Knowles, barriers Syst. geographic without Ecol. breaks Phylogeographic Rev. 2002. Annu. E. D. selection. Irwin, and Individuality 1980. L. D. Hull, Press, Illinois of University systematics. Phylogenetic 1966. W. Hennig, Pages process. and pattern evolutionary Linking 1998. G. R. Harrison, asi .adO .Ggiti 04 eaouainbooy Past, biology: Metapopulation 2004. Gaggiotti. E. O. and I. Hanski, am- of checklist and classification evolutionary An 2001. L. L. Grismer, 886 ain rnsEo.Eo.9:373–375. Evol. Ecol. Trends vation. 88:207– Bryologist bryophytes. in concepts 214. species of basis genetic J. information. genetic and spatial 96:722–724. Hered. interindividual of analysis joint 4:1–38. York. New Press, University Columbia eds.). Meier, R. and 30–43 Cam- Press, University Harvard Massachusetts. of bridge, Press Belknap inheritance. and Massachusetts. Cambridge, Press, University Harvard Y Massachusetts. Cambridge, Press, University York. New Press, sity 31:95– Nematol. J. puzzle. species the 1 on closure toward Advances eds.). Wilson, London. R. Hall, M. and and Dawah, Chapman A. H. Claridge, F. (M. biodiversity of ntesg fteseispolm ae 381–424 Pages problem. species the of saga the in J. Afr. S. Anderson. isolation. L. versus Recognition 83:534–537. M. species: Sci. and of Allsopp, concept The M. Weissenbacher, 1987. K. B. Ferguson, de- be 76:173–190. Biol. can Hum. barriers algorithm. Monmonier’s How using variation: tected linguistic) morphologic, netic, ge- population 18:189–197. and Evol. ecology Ecol. Trends landscape netics. Combining genetics: scape 10:294–299. Evol. Ecol. So- Island. Mathematical Rhode American Providence, ed.). ciety, Desternhaber, (M. biology in lems delim- 40:435–447. species Evol. help Phylogenet. to Mol. threshold itation. within molecular a divergence of molecular Proposal Crustacea: and taxonomy morphological tween University Hopkins Johns application. Baltimore. Press, and Theory concept: nition issue. 56:This Biol. Syst. trees. gene monophyletic 56:2383–2394. Evolution flow. gene to 1 Urbana. York. New Press, University Oxford eds.). Berlocher, H. 19–31 Elsevier, eds.). Gaggiotti, E. O. and Amsterdam. Hanski (I. metapopulations of rsn,adftr.Pgs3–22 Pages future. and present, 100:12–23. Sci. Acad. Calif. Mexico. California, South. Baja Bull. of islands Pacific the on reptiles and phibians br,T,C .Dud,M oy .Gbr.20.Rltosi be- Relationship 2006. Gibert. J. Gouy, M. Douady, J. C. T., ebure, 16. 1:311–332. ork. in in nls om:Seisadseito D .Hwr,adS. and Howard, J. (D. speciation and Species forms: Endless pce ocpsadpyoeei hoy(.D Wheeler D. (Q. theory phylogenetic and concepts Species rr,adE ee.20.Gorpi atrso (ge- of patterns Geographic 2004. Heyer. E. and erard, in clg,gntc,adevolution and genetics, Ecology, in oemteaia prob- mathematical Some in pce:Teunits The Species: SYSTEMATIC BI aesn .E .18.Tercgiincneto pce.Pgs21– Pages species. of concept recognition The 1985. phylo- H. the E. of H. amplification Paterson, An 1990. Wheeler. D. biogeography. Q. and and C., Systematics K. 1981. Nixon, Platnick. I. N. and G., Nelson, us soit dtr onWiens John Editor: Associate Guest 2007; January 16 returned reviews 2006; November 1 submitted First 381:566. Nature diversity. species Bird 1996. M. R. Zink, W W Va T T bi- in T autocorrelation Spatial 1978b. Oden. L. R. and R., biology R. in autocorrelation Sokal, Spatial 1978a. Oden. L. N. and A R., concept: R. species Sokal, biological The 1970. Crovello. J. T. and R., R. Sokal, variation geographic of significance statistical Testing 1979. R. R. Sokal, prin- The taxonomy: Numerical 1973. Sokal. R. R. and A., H. P. delimiting Sneath, for criteria Operational 2004. Marshall. C. J. and W., renaissance J. A Sites, species: Delimiting 2003. Marshall. C. J. Uni- and W., Columbia J. taxonomy. Sites, animal of Principles 1961. 5:285–298. G. Evolution concept. G. species Simpson, The 1951. G. G. Simpson, of basins intermontane and uplands the from Fishes 1979. E. D. Rosen, species into ecology more Adding Biol. 2007. problem. Apodaca. J. species J. and the J., L. to Rissler, solution cladistic The 1989. M. Ridley, Ap- 2007. Pearson. R. and Rabibisoa, N. Ingram, C. J., C. Raxworthy, S. Duran, P. D. Cardoso, A. Gomez-Zurita, J. Barraclough, G. T. J., Pons, BioEssays concepts. resemblance family as Species 2003. M. Pigliucci, mltn .R 98.Nse ld nlsso hlgorpi data: phylogeographic of analysis clade Nested 1998b. R. A. empleton, popula- Geography, speciation: and Species 1998a. R. A. empleton, ge- A speciation: and species of meaning The 1989. R. A. empleton, ih,S 90 h ttsia osqecso edla heredity Mendelian of consequences statistical The 1940. S. right, ly .O 98 h vltoayseiscnetrcniee.Syst. reconsidered. concept species evolutionary The 1978. O. E. iley, 29 6:211–223. Cladistics concept. species genetic York. New Press, University Columbia uly d) xodUiest rs,London. Press, University 161–183 Oxford Pages ed.). Huxley, speciation. to relation in 27:17–26. Zool. 25:233–239. 7:381–397. Ecol. T Ox- eds.). Berlocher, York. H. New S. Press, and University Howard ford J. (D. speciation and 32–43 Species Pages trees. gene and ecology, structure, tion eds.) Endler, A. J. Massachusetts. and Otte 3–27 10:229– (D. Pages Soc. perspective. Linn. netic of J. applications Biol. four interest. and ecological 249. implications and biological evolutionary Some 2. ology 10:199–228. Soc. Linn. J. Biol. Methodology. 1. 104:127–153. Nat. Am. evaluation. critical 28:227–232. Zool. Syst. patterns. San Freeman, H. W. classification. numerical Francisco. of practice and ciples 35:199–227. Syst. Evol. Ecol. Rev. Annu. species. 18:462–470. Evol. Ecol. Trends biology. systematic in issue York. New Press, versity 162:267–376. Bull. Hist. geography. Nat. Mus. comparative Am. and studies Revisionary Guatemala: issue. ( 56:This salamander Biol. black Syst. the in species de- cryptic help fine phylogeography and models niche Ecological delimitation: 4:1–16. Philos. issue. 56:This A Biol. Syst. delimitation: Madagascar. species for modeling r niche ecological of plications undescribed of taxonomy 55:595–609. DNA Biol. the Syst. Sequence- Insects. 2006. for Vogler. P. delimitation A. and species Sumlin, based D. W. Kamoun, S. Hazell, 25:596–602. Pretoria. nV nlacpac 1Ags 2007 August 21 acceptance final LG VOL. OLOGY ve n miia vlainuigdygco ( geckos day using evaluation empirical and eview sighptee bu eeflwadpplto itr.Mol. history. population and flow gene about hypotheses esting in ln .17.Eooia pce,mlipce,adok. oaks. and multispecies, species, Ecological 1976. L. alen, pce n pcain(.S ra d) rnva Museum, Transvaal ed.). Vrba, S. (E. speciation and Species in . pcainadisconsequences its and Speciation iae soits Sunderland, Associates, Sinauer in h e ytmtc (J. systematics new The nie flavipunctatus Aneides in Phelsuma nls forms: Endless )from 56 ).