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Systematic Biology
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Species Concepts and Species Delimitation
Kevin De Queiroz a
a Department of Vertebrate Zoology, 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
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2007
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Syst. DOI: 10.1080/10635150701701083
Biol
.
56(6 Species Concepts and Species Delimitation
):87
9–
886,
200
KEVIN DE QUEIROZ
7 Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution,
Cop
yrig Washington,
ht c DC 20560-0162, USA; E-mail: [email protected]
Soci
ety
of Abstract.— The issue of species delimitation has long been confused with that of species conceptualization,
Syst
emat leading to a half century of controversy concerning both the definition of the species category and methods
ic for inferring the boundaries and numbers of species. Alternative species concepts agree in treating existence
Biol as a separately evolving metapopulation lineage as the primary defining property of the species category,
ogist
s but they disagree in adopting different properties acquired by lineages during the course of divergence (e.g.,
ISS intrinsic reproductive isolation, diagnosability, monophyly) as secondary defining properties (secondary
N: species criteria). A unified species concept can be achieved by treating existence as a separately evolving
106 metapopulation lineage as the only necessary property of species and the former secondary species criteria
3-
515 as different lines of evidence (operational criteria) relevant to assessing lineage separation. This unified
7 concept of species has several consequences for species delimitation, including the following: First, the
print issues of species conceptualization and species delimitation are clearly separated; the former secondary
/
107 species criteria are no longer considered relevant to species conceptualization but only to species
6- delimitation. Second, all of the properties formerly treated as secondary species criteria are relevant to
836 species delimitation to the extent that they provide evidence of lineage separation. Third, the presence of
X
onli any one of the properties (if appropriately interpreted) is evidence for the existence of a species, though
ne more properties and thus more lines of evidence are associated with a higher degree of corroboration.
Fourth, and perhaps most significantly, a unified species concept shifts emphasis away from the traditional
species criteria, encouraging biologists to develop new methods of species delimitation that are not tied to
those properties. [Species concept; species criteria; species delimitation.]

Readers of Systematic Biology hardly need to concepts, and there are even more
be reminded of the importance of species in alternative definitions (where a
biology. Ac-cording to various authors, species definition is a concise description of
are one of the fun-damental units of biology, a concept, so that any given species
making them comparable in importance to concept may be associated with
genes, cells, and organisms, some of the definitions that differ in minor details
fundamental units at lower levels of biological of wording). Many of these concepts
orga-nization (e.g., Mayr, 1982; see also de and their associated definitions are
Queiroz, 2005a). However, because species exist incom-patible in that they can lead to
at a higher level of orga-nization than the different conclusions concerning the
humans observing them, species also are boundaries and numbers of species.
generally much larger and longer lived than their Thus, the species concept problem—
hu-man observers. Moreover, the connections that is, current disagree-ments about
among their parts (i.e., organisms) are the theoretical concept of the species
ephemeral. This makes it more or less —is closely tied to the issue of
impossible for humans to perceive entire species species delimitation—that is, how to
simply by looking at them, as they do for cells determine the boundaries and
and organ-isms, which is why biologists have numbers of species from emperical
symposia devoted to the topic of species data.
delimitation.
To complicate matters, for roughly the past
half cen-tury, the issue of species delimitation
has been confused by a problem involving the
concept of species itself. The problem is that
currently different subgroups of biol-ogists
advocate different and at least partially incom-
patible species concepts (reviewed by Mayden,
1997; de Queiroz, 1998; Harrison, 1998).
Mayden (1997) listed 24 different named species
 Fortunately, this species concept problem is not as seri-ous ALTERNATIVE SPECIES CONCEPTS
as it appears. Despite the obvious differences among Table 1 is a list of alternative species concepts.
contemporary alternative species concepts and defini-tions, The list consists of major categories of alternative
they exhibit an underlying conceptual unity, which provides species con-cepts advocated by contemporary
the basis for a unified concept of species. As a consequence, biologists, with the categories defined in terms of
biologists are now in a position to free our-selves from the properties upon which they are based. Most
seemingly endless debates about the con-cept of species and readers of this journal are likely knowledgeable
thus also the definition of the species category. One of the about at least some of these proposed concepts,
most significant benefits of a uni-fied species concept is that it which include the familiar biological, ecologi-cal,
allows biologists to ap-proach the problem of species evolutionary, and phylogenetic concepts, among
delimitation in a more straightforward way. In this paper, I oth-ers. Importantly, all of these concepts have
will review the species concept problem and a proposal about advocates among contemporary biologists. In
how di-verse species concepts can be unified, which I have addition, many of the concepts are at least partially
incompatible. For ex-ample, several authors have
pub-lished previously (de Queiroz, 1998, 1999, 2005a, 2005b,
called attention to situations in which adoption of
2005c). I will then examine some of the consequences of a the biological species concept leads to the
unified species concept for the problem of species recognition of fewer species taxa than adoption of
delimitation. one of the alternative species concepts, such as the

879
880 SYSTEMATIC BIOLOGY VOL.

diagnosable version of the phylogenetic species ogists who adopt a multidisciplinary approach, or
Downloaded By: [De Queiroz, Kevin] At: 16:01 16 November

concept (e.g., Bremer and Wanntorp, 1979; those who can step back from their own personal
Cracraft, 1983; Zink, 1996). investments and research interests, all of the
The reason for these incompatibilities has to do concepts seem to have some merits. They are all
with the different biological properties upon based on important biological properties.
which several of the alternative concepts are
based; for example, intrinsic reproductive
isolation in the case of the isolation ver-sion of R ECONCILIATION
the biological species concept, occupation of a
distinct niche or adaptive zone in the case of the The Common Element
ecologi-cal species concept, and fixed character As I have argued previously (e.g., de Queiroz,
state differences in the case of the diagnosable 1998, 1999, 2005a, 2005b, 2005c), the key to
version of the phyloge-netic species concept reconciling the alter-native species concepts is
(Table 1). Moreover, these differ-ences in identifying a common element, which implies a
emphasis are to be expected, because the various single, more general, concept of species. Previous
properties are of greatest interest to different attempts to solve the species concept problem
subgroups of biologists. For example, have tended instead to obscure the solution by
reproductive incompatibili-ties are of central empha-sizing the differences, rather than the
importance to biologists who study hybrid zones, similarities, among rival concepts. As it turns out,
niche differences are paramount for ecolo-gists, all contemporary species concepts share a
and diagnosability and monophyly are fundamen- common element and, equally impor-tant, that
tal for systematists. Similarly, morphological shared element is fundamental to the way in which
differences are central for paleontologists and species are conceptualized. The general concept to
museum taxonomists, whereas genetic ones are which I refer equates species with separately
key for population geneticists and molecular evolv-ing metapopulation lineages, or more
systematists. On the other hand, for biol- specifically, with

TABLE 1. Alternative contemporary species concepts (i.e., major classes of contemporary species definitions) and the
properties upon which they are based (modified from de Queiroz, 2005). Properties (or the converses of properties) that
represent thresholds crossed by diverging lineages and that are commonly viewed as necessary properties of species are marked
with an asterisk (*). Note that under the proposal for unification described in this paper, the various ideas summarized in this
table would no longer be considered distinct species concepts (see de Queiroz, 1998, for an alternative terminology). All of
these ideas conform to a single general concept under which species are equated with separately evolving metapopulation
lineages, and many of the properties (*) are more appropriately interpreted as operational criteria (lines of evidence) relevant to
assessing lineage separation.
 Species concept Property(ies) Advocates/references
Biological Interbreeding (natural reproduction resulting in Wright (1940); Mayr (1942); Dobzhansky (1950)
viable and fertile offspring)
Isolation *Intrinsic reproductive isolation (absence of Mayr (1942); Dobzhansky (1970)
interbreeding between heterospecific organisms
based on intrinsic properties, as opposed to
extrinsic [geographic] barriers)
Paterson (1985); Masters et al. (1987); Lambert
Recognition *Shared specific mate recognition or fertilization and
system (mechanisms by which conspecific Spencer (1995)
organisms, or their gametes, recognize one
another for mating and fertilization)
Ecological *Same niche or adaptive zone (all components of Van Valen (1976); Andersson (1990)
the environment with which conspecific
organisms interact)
Evolutionary Unique evolutionary role, tendencies, and Simpson (1951); Wiley (1978); Mayden (1997)
historical fate
(some interpretations) *Diagnosability (qualitative, fixed difference) Grismer (1999, 2001)
Cohesion Phenotypic cohesion (genetic or demographic Templeton (1989, 1998a)
exchangeability)
Phylogenetic Heterogeneous (see next four entries) (see next four entries)
Hennig (1966); Ridley (1989); Meier and
Hennigian Ancestor becomes extinct when lineage splits Willmann
(2000)
Monophyletic *Monophyly (consisting of an ancestor and all of Rosen (1979); Donoghue (1985); Mishler (1985)
its descendants; commonly inferred from
possession of shared derived character states)
Genealogical *Exclusive coalescence of alleles (all alleles of a Baum and Shaw (1995); see also Avise and Ball
given gene are descended from a common (1990)
ancestral allele not shared with those of other
species)
Diagnosable *Diagnosability (qualitative, fixed difference) Nelson and Platnick (1981); Cracraft (1983); Nixon
and Wheeler (1990)
Michener (1970); Sokal and Crovello (1970);
Phenetic *Form a phenetic cluster (quantitative difference) Sneath
and Sokal (1973)
Genotypic cluster (definition) *Form a genotypic cluster (deficits of genetic Mallet (1995)
intermediates; e.g., heterozygotes)

2007 DE QUEIROZ—SPECIES CONCEPTS AND SPECIES DELIMITATION 88

segments of such lineages. To clarify, here the

term lineage refers to an ancestor-descendant
series (Simpson, 1961; Hull, 1980) in this case of
metapopulations or simply a metapopulation
extended through time (cf. Simpson, 1951). It is
not to be confused with a clade or mono-phyletic
group, which is sometimes also called a lineage
but is generally made up of several lineages
(separate branches). The term metapopulation
refers to an inclu-sive population made up of
connected subpopulations (Levins, 1970; Hanski
and Gaggiotti, 2004). It is used here to distinguish
species, which are traditionally con-sidered to
reside at the higher end of the population-level
continuum, from populations at the lower end of
the continuum, such as demes and family groups.
Fi-nally, a species is not an entire metapopulation
lineage but only a segment of such a lineage. The
point here is that species give rise to other species,
thereby form-ing (species level) lineages. Any
gi s share the common view that species are processes: mutation, natural selection, migration
ve (segments of) sepa-rately evolving (or the lack thereof), and genetic drift. The
n metapopulation lineages (for evidence, see de characters affected by those processes, however,
sp Queiroz, 1998), it is instructive to consider how are highly diverse. They may be genotypic or
eci so much disagreement about species concepts can phenotypic; qualitative or quantitative; selectively
es exist in spite of this general conceptual advantageous, disadvantageous, or neutral; and
is agreement. Clarifica-tion emerges when we they may involve many different aspects of
bu consider the differences among alternative species organis-mal biology, including genetics,
t concepts in the context of the com-mon element development, morphol-ogy, physiology, and
on (i.e., the idea that species are separately evolving behavior. With regard to the species concept
e metapopulation lineages). If we consider the problem, the important point is that changes in
of common element to be the primary defining these characters lead to the acquisition of a number
ma property of the species category, then the diversity of different properties by diverging lineages. Thus,
ny of species con-cepts can be accounted for by as the lineages diverge, they (or their component
se positing that many of the properties that underlie organisms) become phenetically distinguishable.
g alternative species concepts (those marked with They become diag-nosable in terms of fixed
me an asterisk in Table 1) have been implicitly character states. Their genitalia, gametes, and
nts treated as secondary defining properties of the developmental systems become incompat-ible.
tha species category. The point is that most of the al- Their mate recognition systems diverge to the
t ternative species concepts adopt different point where the organisms no longer recognize one
ma properties of lineages as secondary defining another as potential mates. They evolve distinctive
ke properties. Thus, under all species concepts, a ecologies. And they pass through polyphyletic,
up species is a separately evolving metapopulation paraphyletic, and mono-phyletic stages in terms of
their component genes. The problem is that these
su lineage, but under the isolation version of the
changes do not all occur at the same time, and they
ch biological species concept, the lineage also has to
do not even necessarily occur in a regular order (de
a be intrinsically reproductively isolated from other
Queiroz, 1998). The reason this is a problem is that
sp lin-eages; under the ecological species concept,
each of several different species concepts adopts a
eci the lineage also has to occupy a different niche;
different property from this set as a defining
es under the phenetic species concept, it also has to (necessary) property of the species category. This
lev be phenetically distinguish-able; under the is the reason that the different species concepts,
el phylogenetic species concept (mono-phyly despite sharing a common fundamental element,
lin version), it also has be monophyletic in terms of can nonetheless lead to different conclusions
ea its component genes, organisms, or concerning which lineages deserve to be rec-
ge. subpopulations, and so forth. ognized as species.
The reason that these different secondary Figure 1 is a highly simplified diagram
properties (secondary species criteria) lead to representing the process of lineage separation and
incompatible species concepts is that they arise at
The Differences divergence (i.e., speciation). The shades of gray
different times during the process of speciation represent the daugh-ter lineages becoming more
G and more different from one another through time,
(here used in a general sense to encompass all of
ive and the numbered lines represent the times at
the phenomena that have been em-phasized by
n contemporary biologists). Speciation can be which they acquire different properties relative to
tha conceptualized in terms of a few general each other—for example, when they become
t evolutionary phenetically distinguishable, diagnosable,
all reciprocally monophyletic, reproductively
co incompatible, ecologically distinct, and so forth.
nte This set of properties forms a large gray zone
m within which alternative species concepts come
po into conflict. On either side of the gray zone, there
rar will be unanimous agreement about the num-ber of
y species. Before the acquisition of the first prop-
sp erty, everyone will agree that there is a single
eci species, and after the acquisition of the last
es property, everyone will agree that there are two. In
co between, however, there will be disagreement. The
nc reason is that each of sev-eral different
ept contemporary species concepts adopts a different
pr ented by the horizontal lines) as its cutoff for somewhat later, perhaps where the lineages
op considering a separately evolving lin-eage to have develop an intrinsic reproductive bar-rier. And still
ert become a species. Thus, some people will draw others will draw the cutoff later yet, per-haps
y the cutoff relatively early in the process of diver- where both lineages form exclusive
(re gence, perhaps where differences in quantitative (monophyletic) groups in terms of multiple gene
pr char-acters make the lineages phenetically trees. This is cause of the
es distinguishable. Others will draw the cutoff
882 SYSTEMATIC BIOLOGY VOL.

agree-ment about the number of species. Before the acquisition

of the first property, everyone will agree that there is a single
2 species, and after the acquisition of the last property, everyone
Specie will agree that there are two. In between, however, there will be
s disagreement. The reason is that different contemporary species
concepts adopt different proper-ties (represented by the
horizontal lines) as their species criteria—that is, as their
cutoffs for considering a separately evolving lineage to have
become a species.
SC
9
species concept problem. This is the reason for the
SC exis-tence of so many incompatible definitions of
8 the species category despite widespread agreement
about the gen-eral nature of species.
SC
7
A Unified Species Concept
SC
Gray Zone 6 The situation I have just described suggests a
(1 vs. 2 simple solution to the species concept problem.
species)
SC The solution in-volves a relatively minor yet still
5 fundamental shift in the way that species are
conceptualized. It retains the el-ement that is
SC
4 common to all contemporary species con-cepts,
and it eliminates the conflicts between those rival
SC concepts without denying the importance of the
3
prop-erties that underlie their obvious differences.
SC In short, it represents a unified species concept.
2

SC
1

1
Specie
s

FIGURE 1. Lineage separation and divergence (speciation)

and species concepts (after de Queiroz, 1998, 1999, 2005a).
This highly sim-plified diagram represents a single lineage
(species) splitting to form two lineages (species). The
gradations in shades of gray represent the daughter lineages
diverging through time, and the horizontal lines la-beled SC
(species criterion) 1 to 9 represent the times at which they
acquire different properties (i.e., when they become
phenetically dis-tinguishable, diagnosable, reciprocally
monophyletic, reproductively incompatible, ecologically
distinct, etc.). The entire set of properties forms a gray zone
within which alternative species concepts come into conflict.
On either side of the gray zone, there will be unanimous
 T ept of species as separately evolving lineages. These properties, attributes such as
he metapopulation lineages (or, more properly, phenetic distinguishabil-ity, reciprocal
sol segments thereof). Second, it treats this property monophyly, pre- and postzygotic repro-ductive
uti as the only necessary property of species. In other isolation, and so forth, are all properties that
on words, all the other properties that have lineages acquire as they separate and diverge from
has previously been treated as necessary properties of one another and therefore provide evidence of
tw species—the properties that created the lineage separation and divergence. Because
o incompatibilities among alter-native species species are con-ceptualized as (segments of)
co concepts—are reinterpreted as no longer being separately evolving lin-eages, evidence of lineage
mp defining (necessary) properties of the species separation is evidence for the existence of
on cate-gory. Instead, they are considered contingent different species. Thus, the properties in question
ent properties: properties that species may or may not remain directly relevant to the issue of species
s. acquire during the course of their existence. In delimitation.
Fir other words, lineages do not have to be
st, phenetically distinguishable, diagnos-able, A second way in which these properties remain
it monophyletic, intrinsically reproductively im-portant is that they can be used to define
ret isolated, ecologically divergent, or anything else subcategories of the species category—that is, to
ain to be considered species. They only have to be recognize different classes of species based on the
s evolving separately from other lineages. If this properties that those species possess. However, in
the proposal is accepted, then it is no longer contrast to the way that classes of species have
co appropriate to refer to the ideas in question (Table been named under the alterna-tive species
m 1) as different species concepts, and a revised ter- concepts—that is, using overly general and
mo minology is needed (see de Queiroz, 1998). therefore misleading adjectives (e.g., biological
n Despite denying that certain properties are species, ecological species, phylogenetic species
ele necessary properties of species, an important part etc.)—a more precise and therefore more useful
me of the reason that the species concept resulting terminology can be developed under the unified
nt from the aforemen-tioned proposal can be species concept using ad-jectives that describe the
— considered unified is that it continues to embrace properties of interest (e.g., re-productively isolated
the the various properties that have been considered species, ecologically differentiated species,
ge important under the rival species con-cepts. Those monophyletic species, etc.). Subcategories of the
ner properties—the former secondary species criteria species category are important in that they are
al —remain important in two ways. First, they serve composed of those species that are relevant to
co as important operational criteria or lines of addressing partic-ular biological questions. For
nc evidence relevant to assessing the separation of example, a study of re-inforcement (Butlin 1987)
requires species that exhibit
2007 DE QUEIROZ—SPECIES CONCEPTS AND SPECIES DELIMITATION 88

postmating reproductive incompatibilities, whereas

a study that uses a species-level phylogeny to
make in-ferences about historical biogeography
might be better served using species that exhibit
monophyly. In any case, the point is that a unified
species concept would continue to embrace all of
the properties that have been consid-ered
important by previous authors; it just would not
treat any of those properties as necessary
properties of species.
It is appropriate to point out here that the unified
species concept just described is not a new species
con-cept but simply the clear separation of the
theoretical concept of species (as separately
evolving metapopula-tion lineages) from
operational criteria (lines of evidence) that are
used for its empirical application. As such, it is not
surprising that several previously proposed charac-
ter population concept” (e.g., Wright, 1940; Mayr, of defining the species category (species
iza 1942; Dobzhansky, 1950) and later (e.g., Mayr, conceptualiza-tion) from the methodological
tio 1969, 1970) the “biological species con-cept” problem of inferring the boundaries and numbers
ns referred, at least initially, to a general theoretical of species (species delimita-tion). Previously these
of concept of species (though restricted to sexually two issues were commonly con-fused in that the
the repro-ducing organisms) that should not be same properties that were used to infer species
sp confused with Mayr’s popular species definition, boundaries and numbers were also considered
eci which incorporates the operational criterion of necessary for a lineage to be regarded as a species
es intrinsic reproductive isola-tion (de Queiroz, (i.e., for deciding when a lineage had diverged
cat 2005a). Similarly, the species definitions of enough to be con-sidered a species). Moreover,
eg Simpson (1951, 1961) and Wiley (1978) do not because different authors considered different
or include operational criteria and thus correspond
properties to be necessary, they commonly
y closely to the unified species concept (de Queiroz,
disagreed about the boundaries and numbers of
co 1998, 1999). More-over, Mayden (1997, 1999)
species. In other words, the issue of species delim-
rre has recognized both that these characterizations
sp represent a common general concept of species itation was intimately intertwined with that of
on and that many of the alternative views are dis- species conceptualization and hopelessly confused
d tinguished primarily by operational criteria. by disagree-ments about the species concept.
clo Hennig’s (1966) characterization of species is In contrast, under a unified species concept, the
sel similar to the gen-eral biological species concept. prop-erties in question are no longer considered
y Its distinctive property— the extinction of necessary properties of species. This situation
to ancestral species when they give rise to clarifies the issue of species delimitation by
the descendant species—was adopted in the interests revealing that those proper-ties have nothing to do
un of strict conformity to a nested, hierarchical with the conceptual problem of defining the
ifi model (Hennig, 1966:64; Meier and Willmann, species category. Instead, they are more
ed 2000) and is not an opera-tional criterion for appropriately viewed as lines of evidence relevant
sp deciding when a lineage is sufficiently divergent to the fundamentally different methodological
eci to be considered a species. And finally, the (rather than conceptual) problem of inferring the
es properties that Templeton (1989) identified as boundaries and numbers of species—that is,
co cohesion mechanisms relevant to his species species delimitation. Thus, under a unified concept
nc definition, though related to several operational of species, there should no longer be any
ept species criteria, represent phenomena that are disagreements about the boundaries and numbers
. hypothesized to be responsible for the existence of species that result purely from disagreements
Th of metapopulation lineages (see Pigliucci, 2003; about the definition of the species category.
us, de Queiroz, 2005c). Instead, disagree-ments about species delimitation
the should result from dis-agreements or differences
ide concerning one or more of the following issues:
as CONSEQUENCES FOR SPECIES DELIMITATION the reliability of particular meth-ods (i.e., for
A unified species concept has consequences for inferring lineage separation), the relevance of
tha
particular data, temporal scale (years versus
t the issue of species delimitation, some of which I
decades versus centuries, etc.), prospective versus
M will briefly describe in the remainder of this
retrospective perspectives, and cases of incomplete
ay paper. lineage separation.
r
(1
96 Conceptualization versus Delimitation
Relevance of Diverse Properties
3) One of the most important consequences of a
Another consequence of a unified species
ter unified species concept is that it clarifies the issue
concept is that many different properties are
me of species de-limitation by clearly separating the
conceptual problem relevant to the issue of species delimitation. Under
d
most of the alternative species concepts, in which
the
various properties acquired by diverging lineages
“in
ter were viewed as necessary proper-ties of species, a
br different one of these properties was con-sidered
ee necessary under each alternative concept. This
di practice created the undesirable situation in which
ng each alternative species concept unduly
- emphasized only one of the various properties at
the expense of the others (Bush, 1995), with
bi gaged in an ongoing bat-tle over which property context of a unified species concept, any property
ol was to be considered the most important. that provides evidence of lineage separa-tion is
og relevant to inferring the boundaries and numbers
In contrast, under a unified species concept, of species. Considering the properties that have
ist most of the properties emphasized under the
s previ-ously been adopted as secondary species
alternative con-cepts should be considered criteria (those
en relevant to the issue of species delimitation. In the
884 SYSTEMATIC BIOLOGY VOL.

marked with an asterisk in Table 1), either the constitute evidence contradicting a hypothesis of
prop-erty itself (intrinsic reproductive isolation, lineage separation. In other words, a lineage might
monophyly, exclusive coalescence, lack one or more of those prop-erties even if it is
diagnosability, deficits of genetic intermediates), evolving separately from all other lin-eages. The
or its converse (incompatible fertiliza-tion reason, of course, is that the lineage simply may
systems, different niches, phenetic not yet have evolved the properties, as might be
distinguishabil-ity), provides evidence of lineage expected if it is still in the early stages of
separation. Thus, all of those properties are divergence. Thus, an asymmetry exists concerning
relevant (as lines of evidence) to the problem of the evidence pro-vided by the properties in
species delimitation. question: the presence of any one of those
properties constitutes evidence for lineage
separation, but the absence of the same property
Quantity of Evidence does not constitute evidence against lineage
Viewing the properties in question as evidence separation—that is, against the hypothesis of
of lin-eage separation has additional separate species. When consid-ering only the
consequences. One is that any evidence of lineage properties in question, only the absence of all of
separation is sufficient to in-fer the existence of those properties should be considered evidence
separate species (compare Mayden, 1999). To the against the hypothesis that two (or more) sets of
extent that the possession (by a set of popu- popula-tions represent different species, but even
lations) of even a single relevant property this is negative evidence. On the other hand, it
provides such evidence, it may be considered would seem to go with-out saying that recognizing
a species is inappropriate in the absence of any
evidence for the existence of a species. This is not
positive evidence for its existence.
to say that the properties are in-fallible; on the
contrary, any line of evidence can be mis-leading
if interpreted inappropriately. For example, the
existence of separate species is commonly
inferred from reciprocal monophyly of the alleles
at a given locus in allopartically or parapatrically
distributed sets of popu-lations (e.g., Moritz,
1994; Avise and Wollenberg, 1997). However, if
the locus is maternally inherited, as in the case of
mitochondrial DNA, then a pattern of recipro-cal
monophyly can also result from low dispersal dis-
tances of females even when autosomal and
paternally inherited genes are being exchanged
regularly between the same sets of populations
(e.g., Irwin, 2002). In other words, two or more
species might be inferred from such data even
though the populations in question form a sin-gle
metapopulation lineage. Thus, the point is not that
the presence of a single property guarantees that a
set of populations possessing that property
represents a sepa-rate lineage (i.e., a species) but
only that the presence of a single property
constitutes evidence (which is always fallible)
supporting that hypothesis.
On the other hand, the absence of any one or
more of the properties in question does not
 A corroborated hy-pothesis of lineage separation monophyly, and the like are cer-tainly relevant to
lth (i.e., of the existence of separate species) requires the issue of lineage separation, many of them
ou multiple lines of evidence. In general, the farther represent somewhat artificial cutoffs in the con-
gh along lineages are in the process of divergence, tinuous process of divergence. Moreover, most of
pre the larger the number of differences they can be these properties are not very useful for detecting
sen expected to have acquired relative to one another, lineage sep-aration in the early stages of
ce and therefore the easier it should be to find divergence. In this context, the development of
of evidence of separation. Conversely, the earlier new methods to test hypotheses of lineage
a lineages are in the process of divergence, the separation that are no longer based on the tra-
sin more difficult it should be to find evidence of ditional species criteria represents significant
gle separation. In any case, multiple lines of evidence progress. For example, consider new methods for
pro —that is, the possession of several proper-ties species delimi-tation being developed in the
per that arise during lineage divergence—result in context of coalescent the-ory (e.g., Knowles and
ty more highly corroborated hypotheses of lineage Carstens, 2007). These methods use information
pro separation, and thus of the existence of different from gene trees, which is the same sort of
species. This point may seem obvious, and some information that is commonly used to assess
vid
people have been using multiple lines of evidence mono-phyly under monophyletic and genealogical
es
for years. Nonetheless, the ex-istence of rival versions of the so-called phylogenetic species
evi
species concepts has worked against these efforts concept. However, in the case of these new
-
coalescent-based methods, mono-phyly is not the
de by effectively asking people to choose a preferred
focus. In fact, the methods in question can provide
nc (single) operational criterion.
evidence for lineage separation even when none of
e the sampled loci exhibits monophyly within the
for sets of populations under consideration (Knowles
Alternatives to the Traditional
lin and Carstens, 2007).
Properties
ea Other new methods relevant to species
ge Among the most important consequences of
delimitation make more direct use of geographic
sep adopting a unified species concept is that, by
information than under traditional approaches.
ara emphasizing sep-arately evolving lineages over
Geographic information is crucial because nearly
tio contingent properties of those lineages, it
all species exhibit geographic variation, and it is
n, encourages biologists to shift their at-tention possible for larger differences to exist between
a away from the traditional species criteria and de- populations within the same old and geographi-
hig velop new methods for species delimitation. cally widespread species than between populations
hly Although properties such as intrinsic reproductive from different but recently separated species (de
isolation, diag-nosability, (reciprocal) Queiroz and
2007 DE QUEIROZ—SPECIES CONCEPTS AND SPECIES DELIMITATION 88

Good, 1997). This situation calls into question all

meth-ods that adopt as an operational criterion a
particular level of divergence, whether derived
from previously studied cases (e.g., Lef´ebure et
al., 2006), theoretical mod-els (e.g., Pons et al.,
2006), or based on a more arbitrary criterion, such
as the threshold beyond which parsimony will no
longer correctly estimate the number of muta-tions
with a probability greater than or equal to 0.95
(e.g., Cardoso and Vogler, 2005). (Such methods
may still be useful for obtaining first
approximations when screen-ing large numbers of
samples from understudied taxa, as in the cited
papers.) Geographic information is neces-sary to
distinguish true discontinuities (i.e., lineage sep-
aration) from differentiation that occurs within
species as the result of phenomena such as clines
and isolation by distance.
 A kal and Oden, 1978a, 1978b; Sokal, 1979), with interminable debates about the definition of the
lth certain exceptions, in-cluding Mantel tests (Sokal, species category. Moreover, it provides a unified
ou 1979) and nested clade anal-ysis (Templeton, context for understanding the relevance of diverse
gh 1998b), such methods are underused. In addition, methods to the problem of species delimitation
the most of the traditional species criteria (Table 1) (i.e., as methods for eval-uating whether sets of
dir do not explicitly incorporate geographic populations constitute separately evolving
ect information. This situation is likely to change lineages) and thus also for integrating the infor-
us with the recent and rapid development of mation provided by different species delimitation
e geographic information system technol-ogy and meth-ods in empirical applications.
of its application to problems involving species (see
ge Raxworthy, 2007; Rissler and Apodaca, 2007).
og More-over, methods that incorporate geographic ACKNOWLEDGMENTS
ra information have recently been proposed that are I thank J. Wiens for organizing the 2006 SSB symposium on
ph not based on tra-ditional operational criteria but species delimitation and for inviting me to contribute this
ic instead are designed to identify abrupt changes in paper. L. Knowles provided valuable information about
inf surfaces defined by (genetic or phenotypic) methods based on coalescent theory, and J. Sites, J. Wiens, and
an anonymous reviewer provided comments on an earlier
or characters that are indicative of at least partial version. I have previously acknowledged the contributions of
ma lineage separation (e.g., Manel et al., 2003; Manni numerous colleagues to the development of my views on
tio et al., 2004; Miller, 2005). I will not say more species concepts (see de Queiroz, 1998, 1999, 2005a, 2005b,
n about these or other new approaches to species 2005c).
in delimitation, several of which will be described
me by other contributors to this issue (see also
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