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ZOOLOGICAL RESEARCH
Species delimitation based on diagnosis and
monophyly, and its importance for advancing
mammalian taxonomy
Eliécer E. Gutiérrez1,2,*, Guilherme S. T. Garbino3
1
Pós-Graduação em Biodiversidade Animal, Departamento de Ecologia e Evolução, Centro de Ciências Naturais e Exatas, Universidade
Federal de Santa Maria, Santa Maria, RS 97105-900, Brazil
2Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington DC 20013-7012, USA
3Pós-graduação, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte,
Minas Gerais 31270-901, Brazil
ABSTRACT
A recently proposed taxonomic classification of extant
ungulates sparked a series of publications that
criticize the Phylogenetic Species Concept (PSC)
claiming it to be a particularly poor species concept.
These opinions reiteratively stated that (1) the two
fundamental elements of the "PSC", i.e., monophyly
and diagnosability, do not offer objective criteria as
to where the line between species should be drawn;
and (2) that extirpation of populations can lead to
artificial diagnosability and spurious recognitions of
species. This sudden eruption of criticism against
the PSC is misleading. Problems attributed to the
PSC are common to most approaches and concepts
that modern systematists employ to establish species
boundaries. The controversial taxonomic propositions
that sparked criticism against the PSC are indeed
highly problematic, not because of the species
concept upon which they are based, but because no
evidence (whatsoever) has become public to support
a substantial portion of the proposed classification.
We herein discuss these topics using examples from
mammals. Numerous areas of biological research
rest upon taxonomic accuracy (including conservation
biology and biomedical research); hence, it is
necessary to clarify what are (and what are not) the
real sources of taxonomic inaccuracy.
Keywords:
Alpha taxonomy; Phylogenetic Species
Concept; Species concepts; Taxonomic inertia;
Taxonomic inflation
INTRODUCTION
A recently proposed taxonomic classification for extant
ungulates (Groves & Grubb, 2011) sparked a series of
publications criticizing the species concept upon which the
classification was based, i.e., Phylogenetic Species Concept
(PSC; Heller et al., 2013; Zachos et al., 2013; Zachos, 2013,
2015; Zachos & Lovari, 2013), albeit previous published
opinions had already presented some of the same arguments
against the PSC (e.g., Frankham et al., 2012; Garnett &
Christidis, 2007; Isaac et al., 2004; Tattersall, 2007). Two
main claims about the PSC have been reiteratively used to
highlight it as a particularly poor species concept: (1) the
two fundamental elements of the PSC, i.e., monophyly and
diagnosability, do not offer objective criteria as to where the
line between species should be drawn; and (2) the extirpation
of populations can lead to artificial diagnosability and spurious
recognitions of species. Moreover, these criticisms portray the
use of the PSC as detrimental to conservation efforts. We
argue that the problems attributed to the PSC are common to
most methodological approaches to species limits and to the
most commonly used species concepts that have been the
basis for the taxonomic classifications of mammals currently in
use. Furthermore, we present evidence that the PSC based
on diagnosability and monophyly as operational criteria has
helped to substantially advance mammalian systematics. In
addition, we show that the recent criticism against Groves
& Grubb’s (2011) ungulate taxonomy is mistakenly focused
on an "alleged poverty" of the PSC (see a brief comment
relevant to this general topic by Tsang et al., 2016, p. 529),
whereas the real cause of taxonomic inflation in that proposed
classification lays on numerous empirical problems.
PHYLOGENETIC SPECIES CONCEPT (PSC)
Before we discuss these matters, we must clarify that the
name “Phylogenetic Species Concept” has been associated
to various concepts (e.g., McKitrick & Zink, 1988; Nixon
& Wheeler, 1990), two of which are central in the
Received: 14 December 2017; Accepted: 12 February 2018; Online:
08 March 2018
*Corresponding author, E-mail: ee.gutierrez.bio@gmail.com
DOI: 10.24272/j.issn.2095-8137.2018.037
Science Press Zoological Research 39(3): 1-8, 2018 1
above-mentioned debate. These concepts can be better
regarded as sets of criteria for species delimitation rather
than "concepts", as proposed by de Queiroz (2007); however,
herein we refer to these sets of criteria as "concepts" only
to facilitate communication by using the same terminology
employed by authors of previous articles. These concepts are
as follows (see summaries by Groves et al., 2017; Zachos,
2016a):
Phylogenetic species concept, diagnosis-based
version (dPSC): “The smallest diagnosable cluster
of individual organisms within which there is a
parental pattern of ancestry and descent ” (Cracraft,
1983, p.170). Subsequently formulated as “...
the smallest aggregation of populations (sexual)
or lineages (asexual) diagnosable by a unique
combination of character states in comparable
individuals (semaphoronts)” (Nixon & Wheeler,
1990). A more recent version states that species
are “. . . the smallest population or aggregation of
populations which has fixed heritable differences
from other such populations or aggregations”
(Groves & Grubb, 2011; see also Groves, 2017).
Phylogenetic species concept, monophyly-based
version (mPSC) “... a geographically constrained
group of individuals with some unique
apomorphous character, is the unit of evolutionary
significance” (Rosen, 1978, p. 176).
A third concept that must be incorporated in the discussion
is as follows (see Groves et al., 2017):
Phylogenetic species concept, diagnosis-and-
monophyly-based version (dmPSC), defined as
“... the smallest diagnosable cluster of individual
organisms forming a monophyletic group within
which there is a parental pattern of ancestry and
descent” (Mayden, 1997, p. 407; McKitrick & Zink,
1988).
DO THESE VERSIONS OF THE PSC OFFER OBJECTIVE
CRITERIA AS TO WHERE THE LINE BETWEEN SPECIES
SHOULD BE DRAWN?
The short answer is “no”, but “no” would also be the answer
if the question were asked with regard to any other species
concept, including the Biological Species Concept (BSC)
when applied to allopatric populations (see Groves, 2012 and
references therein). However, the three phylogenetic species
concepts described above differ importantly regarding the
degree of objectivity with which they can be applied.
With regard to the dPSC (sensu Cracraft, 1983; see
also Eldredge & Cracraft, 1980; Nixon & Wheeler, 1990;
Wheeler & Meier, 2000 and references therein), we agree
with previous criticisms (Heller et al., 2013, 2014; Zachos &
Lovari, 2013, Zachos, 2016a) in that this concept is prone to
promote spurious recognition of mere geographic (including
subspecies) or even individual variants of a single species as
if such variants were each a valid species. This is due to the
high degree of subjectivity and arbitrariness implicit in the task
of judging what characteristics are to be deemed adequate
to diagnose species and distinguishing such characteristics
from those that would simply lead to diagnoses of populations,
or groups thereof, within a single species (but see Wiens
& Servedio, 2000). Species are not phenotypically and
genotypically homogeneous across geography, therefore it
is always the case that various populations within a single
species can be diagnosed. These diagnoses by themselves
must not be a justification to regard such populations as
different species. This limitation of the dPSC is exacerbated
when sample sizes are small, as is often the case for medium
and large mammals. In these cases, a researcher may
erroneously infer the existence of phenotypic discontinuity and
the presence of characteristics enabling the diagnosis of a
sample—the latter based on a set of specimens that at the
time were perceived as worthy of species-level recognition.
However, as more samples are obtained, individuals with
intermediate phenotypes with respect to the putative new
species and other geographic samples may be found. This
would render the putative new species, which was previously
thought to be diagnosable, conspecific with an already
recognized species (e.g., Peres et al., 1996). Examples
of these plausible problems are abundant in the proposed
classification of ungulates by Groves & Grubb (2011) (see
below), but are by no means exclusive to it (e.g., Díaz et
al., 1999, 2002; Fonseca & Pinto, 2004; Solari, 2004; van
Roosmalen et al., 2000, 2007); numerous examples exist
in early contributions to mammalian taxonomy (e.g., Miller,
1912; Pocock, 1941; Robinson & Lyon, 1901), and even the
last decade has seen claims advocating for the recognition
of a species made on the basis of phenotypic diagnoses
of as few as one or two specimens—e.g., Meijaard et al.,
2017 p. 513; see also Mantilla-Meluk (2013) for a monkey
subspecies named on the basis of morphometric data and
pelage coloration from only four specimens. Unfortunately,
in some cases descriptions of species have been carried
out not only with unacceptably small sample sizes but also
merely based on images (illustrations, photos, or both) and
lacking preserved type specimens (see Pine & Gutiérrez,
2018 for a review of cases and problems associated to this
phenomenon). Although no data exist to support the notion
that the collection of a single individual (for it to properly serve
as a preserved holotype) significantly increases the probability
of an already endangered species to become extinct, some
researchers may prefer not to carry out such collection
(e.g., Donegan, 2008; but see Dubois & Nemésio, 2007;
Dubois, 2009), or it may be unfeasible due to impediments
in obtaining collection permits. In such cases, a wide
survey of museum specimens might lead to the discovery
and subsequent use of specimens in taxonomic descriptions.
Undertaking comprehensive surveys of museum specimens
may be disregarded by describers of new species, but the
possible data yielded, which may be coupled with photos
of living animals, might ameliorate the detrimental effects of
extremely small sample sizes and help in unveiling geographic
and non-geographic (ontogenetic, sexual) variation (e.g.,
Garbino et al., 2016).
The second concept, the mPSC, under which species must
be both monophyletic and geographically restricted, seems
indefensible. Within a species there can be large numbers
of monophyletic groups that are geographically restricted only
due to recent changes in their environment. An example
of this is the populations of brocket deer of the Cordillera
2www.zoores.ac.cn
de Mérida, Venezuela, which for decades were recognized
as a valid species, Mazama bricenii. This recognition was
based on no data whatsoever and on the assumption of
a plausible differentiation due to its supposed geographic
isolation. However, a recent study that employed ecological
niche modeling found that, if these populations were truly
isolated in modern time, such isolation commenced not long
ago (Gutiérrez et al., 2015). The study also found that while
the focal population formed a monophyletic haplogroup, it
was embedded within a larger (yet shallow) clade whose
terminal branches corresponded to Mazama rufina. Results
from that study showed that what was once known as Mazama
bricenii actually corresponds to Mazama rufina (Gutiérrez et
al., 2015), and illustrate how the application of the mPSC
would have led to mistakenly recognize M. bricenii as if it
were a valid species. Such taxonomic recognition would be
a mPSC-based artifact caused by (1) the fact that sequences
obtained from specimens from the Cordillera de Mérida
(where the populations to which the name M. bricenii would
apply occur) were recovered in a monophyletic haplogroup;
and (2) because those populations might be geographically
isolated in modern time.
The third concept, dmPSC, for which species must be
both monophyletic and diagnosable, has been useful for
improving mammalian taxonomy. As previously noted, many
monophyletic groups are found within a single species, and
that monophyly per se does not constitute a criterion to
determine where the line between species should be drawn.
However, it is also true that assessing whether a candidate
species is monophyletic or not provides a fundamental basis
for its potential recognition as a valid species. Recognizing
a polyphyletic taxon as if it were a valid species would be
absurd. On the other hand, in some situations (e.g., species
originating from peripheral isolation) a candidate species
might meet the criteria (i.e., monophyly and diagnosability)
for validity under the dmPSC, but its recognition renders the
species in which the candidate had thus far been included
as paraphyletic. No consensus has been reached as to
whether taxonomists should accept paraphyletic species as
valid, or, alternatively, if taxonomists should recognize as valid
only those that are monophyletic (see Carter et al., 2015;
Crisp & Chandler, 1996; Dias et al., 2005; Ebach et al.,
2006; Freudenstein, 1998; Funk & Omland, 2003; Hörandl,
2006, 2007; Nelson et al., 2003; Nixon & Wheeler, 1990; de
Queiroz & Donoghue, 1988; Zachos, 2014b; Zander, 2007;
see also Funk & Omland, 2003). Discussing these views
requires a much more extensive text and would distract from
the aim of this perspective piece—i.e., clarifying that despite
the recent criticisms made against PSCs, at least one of
these concepts has served to positively advance mammalian
systematics. By requiring monophyly, the application of the
dmPSC secures that a phylogenetic inference is conducted to
describe or revalidate a species, thus decreasing the chances
that polyphyletic groups of populations would be named
as a species. These phylogenetic estimates also provide
frameworks for evaluating alternatives in cases in which the
description or recognition of a clade as a species would
render an already recognized species as paraphyletic. In
such cases, researchers might simply not describe or formally
recognize that clade at all—which might be acceptable, as
not every clade in a phylogenetic tree represents a taxon
worth naming—or describe it at the subspecies level—with
paraphyly persisting at a lower taxonomic rank—or describe
it and accept paraphyletic species as valid, in which case
the researcher could not invoke any species concept that
requires monophyly (including the dmPSC) upon which to
base the description. Whichever of these alternatives
the researcher prefers, and attempts to justify, due to
philosophical, pragmatic, or both considerations, the fact that
the dmPSC requires a phylogenetic estimate is an advantage
over other concepts that do not, including the dPSC and the
Biological Species Concept.
The requirement that a candidate species must also be
diagnosable in order to be recognized under the dmPSC is
indispensable. A species must have a series of genetically
fixed characteristics that are common to its members and
that serve to distinguish it from other such species. However,
as already discussed (see above), diagnosability alone is, in
general, an inadequate approach to establish species limits.
Acknowledging the existence of the dmPSC is important
because it does represent one of the most explicit methods to
infer species limits—contra authors that ignored the existence
of this concept in their arguments against or in favor of
the "PSC" (e.g., Gippoliti et al., 2018; Groves, 2012, 2017;
Heller et al., 2013; Zachos & Lovari, 2013; Zachos et al.,
2013; Zachos, 2013; Zachos, 2014a, 2015, 2016a). Some
operational steps in delimiting species will always be arbitrary.
In this sense, the advantage of the dmPSC over other
concepts is that its operational criteria for recognition of
species can be objectively tested. In other words, monophyly
and diagnosability are, in general, more easily testable for
allopatric populations than reproductive barriers (BSC), and
more objectively demonstrated than the central criteria upon
which other concepts define species, such as “ecological
roles” in the Ecological Species Concept (Van Valen, 1976).
When applied based on sufficient geographic and taxonomic
sampling, and, ideally (but not strictly necessary; see
below), employing phylogenetic inferences using data from
independent sources (e.g., DNA sequence data obtained from
independently inherited genes), the dmPSC has improved
the taxonomic classifications of various groups of mammals,
some of which remained problematic for decades. Among
studies that exemplify how the dmPSC has helped to advance
mammalian systematics, even if some of them used this
species concept without explicitly or correctly invoking it, are
those on didelphid marsupials (e.g., Díaz-Nieto & Voss, 2016;
Giarla et al., 2010; Gutiérrez et al., 2010; Martínez-Lanfranco
et al., 2014; Pavan et al., 2017; Voss et al., 2018), rodents
(e.g., Hawkins et al., 2016; do Prado & Percequillo, 2017;
Rogers & González, 2010; Voss et al., 2013), bats (e.g., Baird
et al., 2008; Molinari et al., 2017; Moras et al., 2016; Velazco
et al., 2010), and medium and large mammals (e.g., Bornholdt
et al., 2013; Gutiérrez et al., 2015; Helgen et al., 2009, 2013;
Janeˇ
cka et al., 2008; Koepfli et al., 2008; Miranda et al.,
2017; do Nascimento & Feijó, 2017 [and references therein
for phylogenetic evidence]). These studies have not only
unraveled the true-species nature of previously unrecognized
species, but in many cases have shown that taxa considered
as valid species for decades are not valid species at all.
The application of any PSC can promote rampant
taxonomic inflation when applied without sufficient rigor. In
our opinion, this inflation is caused less by philosophical
Zoological Research 39(3): 1-8, 2018 3
aspects and properties of the PSCs and more by empirical
shortcomings. In several studies, geographic and individual
variation do not appear to be satisfactorily addressed, and
names are applied to what could be intraspecific variants
(see examples in Tattersall, 2007). On other occasions,
monophyletic groups recovered from molecular phylogenies
based on sequence data from a single locus promptly receive
new or revalidated names (e.g., Boubli et al., 2012; Thinh
et al., 2010). Nevertheless, it is important to note that
when the established, traditional taxonomic classification of
a focal group is the result of dogmatic acceptance of expert
opinions (often past-century authorities), without support from
data (see Gutiérrez & Helgen, 2013), then even the use
of limited evidence—e.g., analyses of sequence data from
a single locus [despite the well-known shortcomings of this
approach; see Dávalos & Russell, 2014; Knowles & Carstens,
2007; Maddison, 1997], ideally coupled with qualitative and/or
quantitative analyses of morphological data—can well justify
taxonomic changes if based on adequate sampling (e.g.,
Gutiérrez et al., 2010, 2015, 2017; Voss et al., 2013; contra
Zachos, 2009, 2016b).
The proposed ungulate taxonomic classification that
sparked the recent series of criticism against the PSC
is particularly problematic, but not because it was based
on the dPSC. Most controversial aspects of this proposed
classification are not at all associated to any species concept,
as it might seem if one reads the recent debate between Frank
Zachos and Colin Groves and their co-authors with regard
to the "PSC", but rather to more practical aspects of such a
monograph, to name just a few (see also Heller et al., 2013;
Holbrook, 2013; Zachos, 2014a, p. 1): (1) Groves & Grubb
(2011) did not assess geographic variation at all for most of the
species they recognized; (2) unfortunately, for some species
recognized by these authors, the sample size employed was
not indicated nor any published study cited to support the
taxonomic proposals, whereas for many other alleged species
the sample sizes were extremely low—e.g., Alcelaphus tora,
Dorcatragus megalotis,Eudorcas nasalis,Eudorcas tilonura,
Gazella acaciae,Gazella karamii,Gazella shikarii,Lama
mensalis,Madoqua hararensis,Mazama fuscata,Mazama
jucunda,Mazama trinitatis, and Redunca cottoni; (3) no
published phylogenetic information seems to be the basis
of most of their taxonomic propositions; (4) in general, no
detailed discussions were presented on whether recognizing
a taxon as a valid species was more appropriate and justifiable
than regarding it as a subspecies, and it seems that the
objective of the authors was to merely recognize as valid
species as many taxa as possible, without critical evaluation of
alternatives (e.g., recognizing subspecies when appropriate);
(5) a list of the specimens examined was not provided, and
hence it is difficult for the scientific community to evaluate
the authors’ assertions on specimen morphologies based on
the same material with certainty; (6) no data were made
available that would enable reproduction and testability of the
analyses that were the basis of the taxonomic propositions;
(7) although the authors cite published studies for some of
the taxonomic changes they proposed, for others they did
not and nowhere in their monograph can be found results
from any quantitative analyses. We cannot understand why
Groves & Grubb (2011) failed to publish the results of their
quantitative analyses given current possibilities to do so
(see below). Unfortunately, this problem is not unique to
the proposed ungulate taxonomic classification of Groves &
Grubb. An important volume on mammals of South America
(Patton et al., 2015) contained the first modern taxonomic
treatments of various rodent groups (e.g., family Sciuridae,
genera Aepeomys,Oecomys,Rhipidomys,Thomasomys),
but results from analytical procedures assessing geographic
and non-geographic variation of those groups have not been
published (in the book or elsewhere), and in some cases
it seems unlikely they will ever be published. Luckily,
several unpublished Ph.D. dissertations that served as
the basis for the book sections treating those taxa have
been privately shared among colleagues. Clearly, making
these Ph.D. dissertations (and other unpublished material)
digitally available to the scientific community free of charge
from a repository on the Internet (e.g., Dryad, Figshare,
Internet Archive, ResearchGate, Zenodo), if their authors grant
authorization, should be considered by the editors of this book,
and similar actions should be considered by authors and editors
of future monographs introducing taxonomic classifications.
CAN EXTIRPATION OF POPULATIONS LEAD TO ARTIFICIAL
DIAGNOSABILITY AND SPURIOUS RECOGNITIONS OF
SPECIES UNDER THE dmPSC?
The short answer is "it can", but again the same answer
would apply if the question were asked about other species
concepts, including the BSC. In their criticism of the "PSC",
Zachos & Lovari (2013) claimed that the fact that extirpation
of populations can lead to artifactual diagnosability and
monophyly is one of the weaknesses of the PSC that makes
this concept a particularly poor one. They stated that “There
is yet another line of argumentation that clearly shows
the shortcomings of both diagnosability and monophyly
as yardsticks for species delimitation and that we believe
is another coup de grâce for the PSC. Diagnosability
(just like reciprocal monophyly) can and often does occur
as a consequence of extinction of intermediate forms...”.
Unfortunately, Zachos & Lovari (2013) did not realize that
extirpation of intermediate populations is one of the natural
causes of speciation. These events lead to speciation,
affecting gene flow and ecological adaptation of extreme
phenotypes in populations that previously were genetically
connected by the existence of intermediate populations.
In fact, it could be said that living taxa that can be validly
recognized on the planet exist as separate biological entities
and as taxonomically diagnosable units only because of the
extinction of intermediate forms. If all intermediate forms
that have lived since the beginning of life on Earth were
still with us, then all living organisms, from prokaryotes
to eukaryotes and from plants to animals, would exist as
a single morphological and reproductive continuum: no
distinguishable taxa would exist! Logically, in cases in which
extirpations have taken place fairly recently (e.g., due to
human-related causes) no speciation may have yet occurred.
In such cases, the extirpation of populations can potentially
lead to artifactual recognitions of species under the PSCs,
but this issue is far from being associated only to the PSCs;
rather, it is a problem that can potentially affect most, if not
all, species concepts currently in use. For example, this issue
4www.zoores.ac.cn
can lead to artifactual recognition of species under the BSC.
Let us imagine a species, species A, with wide distribution
and showing geographic variation by way of a cline in several
qualitative cranial traits believed to be taxonomically important,
i.e., used by most authors to distinguish species within the
corresponding genus. We will illustrate these traits as color
and shape in polygons that represent populations of species
A (Figure 1, panel 1). If recent extirpations of intermediate
populations take place and only those populations occurring at
the opposite extremes of species A’s range remain as extant,
then these populations will become allopatric and it would
be highly likely that they would be considered as members
of different species under the BSC (Figure 1, panel 2). The
BSC would fail to regard these populations as conspecific,
even employing the approach presented by Tobias et al.
(2010; see also Brooks & Helgen, 2010), which uses the
degree of differentiation known to exist between different but
sympatric species (i.e., species A and B in Figure 1) as a
standard to assess the taxonomic relevance of differentiation
between allopatric populations (i.e., populations of species
A in North and South America in Figure 1)—in order words,
this approach uses the former degree of differentiation as a
threshold at which (or above) allopatric populations could be
treated as different species under the BSC.
Figure 1 Illustration of how population extirpations can promote artifactual recognition of
populations of a single species as if they were different species under the Biological Species
Concept (and many other concepts)
Species A, which is represented by quadrilaterals (rectangle and rectangle-like polygons),
possesses a wide distribution and geographic variation by way of a cline in several qualitative
cranial traits considered taxonomically important; herein these traits are illustrated as color and
shape of the polygons (panel 1). Species B, which is represented by circles, is restricted to North
America, where it occurs in sympatry with some North American populations of species A
(panel 1). If extirpation of populations of species A takes place and only those populations
occurring at the opposite extremes of species A's range remain as extant, then these populations
will become allopatric (panel 2). In that scenario, it would be highly likely that the remaining
extant populations would be considered as members of a different species under the BSC (panel
2). The BSC would fail to regard these populations as conspecific, even employing the approach
Figure 1 Illustration of how population extirpations can promote artifactual recognition of populations of a single species as if
they were different species under the Biological Species Concept (and many other concepts)
Species A, which is represented by quadrilaterals (rectangle and rectangle-like polygons), possesses a wide distribution and geographic variation by way of
a cline in several qualitative cranial traits considered taxonomically important; herein these traits are illustrated as color and shape of the polygons (panel 1).
Species B, which is represented by circles, is restricted to North America, where it occurs in sympatry with some North American populations of species A
(panel 1). If extirpation of populations of species A takes place and only those populations occurring at the opposite extremes of species A’s range remain
as extant, then these populations will become allopatric (panel 2). In that scenario, it would be highly likely that the remaining extant populations would be
considered as members of a different species under the BSC (panel 2). The BSC would fail to regard these populations as conspecific, even employing the
approach presented by Tobias et al. (2010; see also Brooks & Helgen, 2010), which uses the degree of differentiation known to exist between different but
sympatric species (i.e., species A and B) as a standard to assess the taxonomic relevance of differentiation between allopatric populations (i.e., populations
of species A in North and South America).
CONCLUSIONS
Major differences exist among the different concepts labeled
as the "Phylogenetic Species Concept", and the one that
uses both diagnosis and monophyly (dmPSC) to delimit
species has been, and will continue to be, important for
positively advancing mammalian taxonomy. Our preceding
discussion should rectify misunderstandings that could arise
from claims made in recently published opinions debating
alleged pros and cons of the "PSC". Although we partially
agree with some of the arguments presented by participants
of that debate, the proposed taxonomic classification of
ungulates (Groves & Grubb, 2011) that motivated this debate
is highly deficient, in our view, not so much because of the
species concept it employed (i.e., dPSC), but rather due to
serious empirical problems. Among them is the absence
of statistical assessments of geographic and non-geographic
variation in diagnostic traits. Although in many instances
the number of specimens available in museums should have
Zoological Research 39(3): 1-8, 2018 5
permitted statistically satisfactory assessments of geographic
and non-geographic variation, results from those analyses
were not presented by Groves & Grubb (2011) in their
monograph. In other instances, extremely low sample sizes
precluded proper statistical analyses.
To refrain from producing taxonomic hypotheses because
of limited material (e.g., few available museum specimens)
would hamper progress in medium and large mammal
taxonomy. As previously mentioned, collecting new samples
of such mammals can be logistically impracticable, and
some researchers may simply prefer not to collect them
due to conservation concerns (but see clarification above).
Thus, even when the available material consists of only a
few specimens, taxonomic studies should still be carried
out, but the taxonomist should bear in mind the statistical
limitations of a small sample, such as inadequate estimations
of population ranges and lower confidence levels. Collating
information from multiple data sources, such as nucleotide
sequences, discrete and continuous morphological data,
and behavior—an approach nowadays called “integrative
taxonomy” (e.g., Dayrat, 2005)—has long been considered
useful as it theoretically increases the probability of correctly
identifying and delimiting taxonomic entities (Simpson, 1961;
Tinbergen, 1959).
Numerous areas of biological research rest upon taxonomic
accuracy (including conservation biology and biomedical
research); hence, it is necessary to clarify what are (and what
are not) the real sources of taxonomic inaccuracy.
COMPETING INTERESTS
The authors declare they have no competing interests.
AUTHORS’ CONTRIBUTIONS
The writing of a first draft of the manuscript was led by E.E.G. Both authors
substantially contributed to all aspects of this publication.
ACKNOWLEDGEMENTS
We thank the editor and two anonymous reviewers for their comments,
which helped improve an earlier version of the now-published manuscript.
We are thankful to our colleagues Kai He, Xue-Long Jiang, and Masaharu
Motokawa for their invitation to contribute to this special issue on mammal
biodiversity of Asia.
REFERENCES
Baird AB, Hillis DM, Patton JC, Bickham JW. 2008. Evolutionary history
of the genus Rhogeessa (Chiroptera: Vespertilionidae) as revealed by
mitochondrial DNA sequences. Journal of Mammalogy, 89(3): 744–754.
Bornholdt R, Helgen K, Koepfli KP, Oliveira L, Lucherini M, Eizirik E. 2013.
Taxonomic revision of the genus Galictis (Carnivora: Mustelidae): species
delimitation, morphological diagnosis, and refined mapping of geographical
distribution. Zoological Journal of the Linnean Society, 167(3): 449–472.
Boubli JP, Rylands AB, Farias IP, Alfaro ME, Alfaro JL. 2012. Cebus
phylogenetic relationships: a preliminary reassessment of the diversity of
the untufted capuchin monkeys. American Journal of Primatology, 74(4):
381–393.
Brooks TM, Helgen KM. 2010. Biodiversity: a standard for species. Nature,
467(7315): 540–541.
Carter JG, Altaba CR, Anderson LC, Campbell DC, Fang ZJ, Harries PJ,
Skelton PW. 2015. The paracladistic approach to phylogenetic taxonomy.
Lawrence, Kansas, USA: Paleontological Institute, 1–9.
Cracraft J. 1983. Species concepts and speciation analysis. In: Johnston
RF. Current Ornithology. Boston, MA: Springer, 159–187.
Crisp MD, Chandler GT. 1996. Paraphyletic species. Telopea, 6(4):
813–844.
Dávalos LM, Russell AL. 2014. Sex-biased dispersal produces high error
rates in mitochondrial distance-based and tree-based species delimitation.
Journal of Mammalogy, 95(4): 781–791.
Dayrat B. 2005. Towards integrative taxonomy. Biological Journal of the
Linnean Society, 85(3): 407–415.
Dias P, Assis LCS, Udulutsch RG. 2005. Monophyly vs. paraphyly in plant
systematics. Taxon, 54(4): 1039–1040.
Díaz MM, Barquez RM, Braun JK, Mares MA. 1999. A new species of
Akodon (Muridae: Sigmodontinae) from northwestern Argentina. Journal
of Mammalogy, 80(3): 786–798.
Díaz MM, Flores DA, Barquez RM. 2002. A new species of gracile
mouse opossum, genus Gracilinanus (Didelphimorphia: Didelphidae), from
Argentina. Journal of Mammalogy, 83(3): 824–833.
Díaz-Nieto JF, Voss RS. 2016. A revision of the didelphid marsupial genus
Marmosops, Part 1. Species of the subgenus Sciophanes.Bulletin of the
American Museum of Natural History, 402: 1–70.
Donegan TM. 2008. New species and subspecies descriptions do not and
should not always require a dead type specimen. Zootaxa, 1761: 37–48.
Dubois A, Nemésio A. 2007. Does nomenclatural availability of nomina
of new species or subspecies require the deposition of vouchers in
collections? Zootaxa, 1409: 1–22.
Dubois A. 2009. Endangered species and endangered knowledge. Zootaxa,
2201: 26–29.
Ebach MC, Williams DM, Morrone JJ. 2006. Paraphyly is bad taxonomy.
Taxon, 55(4): 831–832.
Eldredge N, Cracraft J. 1980. Phylogenetic Patterns and the Evolutionary
Process: Method and Theory in Comparative Biology. New York: Columbia
University Press.
Fonseca RM, Pinto CM. 2004. A new Lophostoma (Chiroptera:
Phyllostomidae: Phyllostominae) from the Amazonia of Ecuador.
Occasional Papers of the Museum of Texas Tech University, Texas: Texas
Tech University, 242: 1–11.
Frankham R, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC,
Mendelson JR, Porton IJ, Ralls K, Ryder OA. 2012. Implications of different
species concepts for conserving biodiversity. Biological Conservation, 153:
25–31.
Freudenstein JV. 1998. Paraphyly, ancestors, and classification: a response
to Sosef and Brummitt. Taxon, 47(1): 95–104.
Funk DJ, Omland KE. 2003. Species-level paraphyly and polyphyly:
frequency, causes, and consequences, with insights from animal
mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics,
34: 397–423.
Garbino GST, Rezende GC, Valladares-Padua C. 2016. Pelage variation
and distribution of the black lion tamarin, Leontopithecus chrysopygus.
Folia Primatologica,87(4): 244–261.
Garnett ST, Christidis L. 2007. Implications of changing species definitions
for conservation purposes. Bird Conservation International, 17(3): 87–195.
Giarla TC, Voss RS, Jansa SA. 2010. Species limits and phylogenetic
relationships in the didelphid marsupial genus Thylamys based on
mitochondrial DNA sequences and morphology. Bulletin of the American
6www.zoores.ac.cn
Museum of Natural History, 346: 1–67.
Gippoliti S, Cotterill FPD, Zinner D, Groves CP. 2018. Impacts of taxonomic
inertia for the conservation of African ungulate diversity: an overview.
Biological Reviews, 93(1): 115–130.
Groves C. 2012. Species concept in primates. American Journal of
Primatology, 74(8): 687–691.
Groves C. 2017. Phylogenetic species concept. In: Fuentes A. The
International Encyclopedia of Primatology. Hoboken, NJ: John Wiley &
Sons, Inc., 1–2.
Groves CP, Grubb P. 2011. Ungulate Taxonomy. Baltimore: Johns Hopkins
University Press.
Groves CP, Cotterill FPD, Gippoliti S, Robovský J, Roos C, Taylor PJ, Zinner
D. 2017. Species definitions and conservation: a review and case studies
from African mammals. Conservation Genetics, 18(6): 1247–1256.
Gutiérrez EE, Jansa SA, Voss RS. 2010. Molecular systematics of
mouse opossums (Didelphidae: Marmosa): assessing species limits
using mitochondrial DNA sequences, with comments on phylogenetic
relationships and biogeography. American Museum Novitates, 3692: 1–22.
Gutiérrez EE, Helgen KM. 2013. Outdated taxonomy blocks conservation.
Nature, 495(7441): 314.
Gutiérrez EE, Helgen KM, McDonough MM, Bauer F, Hawkins MTR,
Escobedo-Morales LA, Patterson BD, Maldonado JE. 2017. A gene-tree
test of the traditional taxonomy of American deer: the importance of
voucher specimens, geographic data, and dense sampling. ZooKeys, 697:
87–131.
Gutiérrez EE, Maldonado JE, Radosavljevic A, Molinari J, Patterson BD,
Martínez-C JM, Rutter AR, Hawkins MTR, Garcia FJ, Helgen KM. 2015.
The taxonomic status of Mazama bricenii and the significance of the
Táchira depression for mammalian endemism in the cordillera de Mérida,
Venezuela. PLoS One, 10(6): e0129113.
Hawkins MTR, Helgen KM, Maldonado JE, Rockwood LL, Tsuchiya MTN,
Leonard JA. 2016. Phylogeny, biogeography and systematic revision of
plain long-nosed squirrels (genus Dremomys, Nannosciurinae). Molecular
Phylogenetics and Evolution, 94: 752–764.
Helgen KM, Kays R, Helgen LE, Tsuchiya-Jerep MTN, Pinto CM, Koepfli
KP, Eizirik E, Maldonado JE. 2009. Taxonomic boundaries and geographic
distributions revealed by an integrative systematic overview of the mountain
coatis, Nasuella (Carnivora: Procyonidae). Small Carnivore Conservation,
41: 65–74.
Helgen KM, Pinto CM, Kays R, Helgen LE, Tsuchiya MTN, Quinn A, Wilson
DE, Maldonado JE. 2013. Taxonomic revision of the olingos (Bassaricyon),
with description of a new species, the Olinguito. ZooKeys, 324: 1–83.
Heller R, Frandsen P, Lorenzen ED, Siegismund HR. 2013. Are there really
twice as many bovid species as we thought? Systematic Biology, 62(3):
490–493.
Heller R, Frandsen P, Lorenzen ED, Siegismund HR. 2014. Is diagnosability
an indicator of speciation? Response to "Why one century of phenetics is
enough”. Systematic Biology, 63(5): 833–837.
Holbrook LT. 2013. Taxonomy interrupted. Journal of Mammalian Evolution,
20(2): 153–154.
Hörandl E. 2006. Paraphyletic versus monophyletic taxa-evolutionary
versus cladistic classifications. Taxon, 55(3): 564–570.
Hörandl E. 2007. Neglecting evolution is bad taxonomy. Taxon, 56(1): 1–5.
Isaac NJB, Mallet J, Mace GM. 2004. Taxonomic inflation: its influence
on macroecology and conservation. Trends in Ecology & Evolution, 19(9):
464–469.
Janeˇ
cka JE, Helgen KM, Lim NTL, Baba M, Izawa M, Boeadi, Murphy
WJ. 2008. Evidence for multiple species of Sunda colugo. Current Biology,
18(21): R1001–R1002.
Knowles LL, Carstens BC. 2007. Delimiting species without monophyletic
gene trees. Systematic Biology, 56(6): 887–895.
Koepfli KP, Kanchanasaka B, Sasaki H, Jacques H, Louie KDY, Hoai T,
Dang NX, Geffen E, Gutleb A, Han SY, Heggberget TM, LaFontaine L, Lee
H, Melisch R, Ruiz-Olmo J. 2008. Establishing the foundation for an applied
molecular taxonomy of otters in Southeast Asia. Conservation Genetics,
9(6): 1589–1604.
Maddison WP. 1997. Gene trees in species trees. Systematic Biology, 46(3):
523–536.
Mantilla-Meluk H. 2013. Subspecific variation: an alternative biogeographic
hypothesis explaining variation in coat color and cranial morphology in
Lagothrix lugens (Primates: Atelidae). Primate Conservation, 26: 33–48.
Martínez-Lanfranco JA, Flores D, Jayat JP, d’Elía G. 2014. A new species
of lutrine opossum, genus Lutreolina Thomas (Didelphidae), from the South
American Yungas. Journal of Mammalogy, 95(2): 225–240.
Mayden RL. 1997. A hierarchy of species concepts: the denouement in
the saga of the species problem. In: Claridge MF, Dawah HA, Wilson MR.
Species: The Units of Biodiversity. London: Chapman & Hall, 381–423.
McKitrick MC, Zink RM. 1988. Species concepts in ornithology. The Condor,
90(1): 1–14.
Meijaard E, Chua MAH, Duckworth JW. 2017. Is the northern
chevrotain, Tragulus williamsoni Kloss, 1916, a synonym or one of the
least-documented mammal species in Asia? Raffles Bulletin of Zoology,
65: 506–514.
Miller GS. 1912. A small collection of bats from Panama. Proceedings of
the United States National Museum, 42(1882): 21–26.
Miranda FR, Casali DM, Perini FA, Machado FA, Santos FR. 2017.
Taxonomic review of the genus Cyclopes Gray, 1821 (Xenarthra, Pilosa),
with the revalidation and description of new species. Zoological Journal of
the Linnean Society, doi: 10.1093/zoolinnean/zlx079/4716749.
Molinari J, Bustos XE, Burneo SF, Camacho MA, Moreno SA, Fermín G.
2017. A new polytypic species of yellow-shouldered bats, genus Sturnira
(Mammalia: Chiroptera: Phyllostomidae), from the Andean and coastal
mountain systems of Venezuela and Colombia. Zootaxa, 4243(1): 75–96.
Moras LM, Tavares VC, Pepato AR, Santos FR, Gregorin R. 2016.
Reassessment of the evolutionary relationships within the dog-faced bats,
genus Cynomops (Chiroptera: Molossidae). Zoologica Scripta, 45(5):
465–480.
do Nascimento FO, Feijó A. 2017. Taxonomic revision of the tigrina
Leopardus tigrinus (Schreber, 1775) species group (Carnivora, Felidae).
Papéis Avulsos de Zoologia (São Paulo), 57(19): 231–264.
Nelson G, Murphy DJ, Ladiges PY. 2003. Brummitt on paraphyly: a
response. Taxon, 52(2): 295–298.
Nixon KC, Wheeler QD. 1990. An amplification of the phylogenetic species
concept. Cladistics, 6(3): 211–223.
Patton JL, Pardiñas UFJ, D’Elía G. 2015. Mammals of South America,
volume 2: Rodents. Chicago, London: University of Chicago Press.
Pavan SE, Mendes-Oliveira AC, Voss RS. 2017. A new species of
Monodelphis (Didelphimorphia: Didelphidae) from the Brazilian amazon.
American Museum Novitates, 3872: 1–20.
Peres CA, Patton JL, Da Silva MNF. 1996. Riverine barriers and gene flow
in Amazonian saddle-back tamarins. Folia Primatologica, 67(3): 113–124.
Pine RH, Gutiérrez EE. 2018. What is an ‘extant’ type specimen? Problems
Zoological Research 39(3): 1-8, 2018 7
arising from naming mammalian species-group taxa without preserved
types. Mammal Review. DOI: 10.1111/mam.12108
Pocock RI. 1941. The races of the ocelot and the margay. Field Museum of
Natural History, Zoological Series,27: 319–369.
do Prado JR, Percequillo AR. 2017. Systematic studies of the genus
Aegialomys Weksler et al., 2006 (Rodentia: Cricetidae: Sigmodontinae):
geographic variation, species delimitation, and biogeography. Journal of
Mammalian Evolution, doi: 10.1007/s10914-016-9360-y.
de Queiroz K, Donoghue MJ. 1988. Phylogenetic systematics and the
species problem. Cladistics, 4(4): 317–338.
de Queiroz K. 2007. Species concepts and species delimitation. Systematic
Biology, 56(6): 879–886.
Robinson W, Lyon Jr MW. 1901. An annotated list of mammals collected
in the vicinity of La Guaira, Venezuela. Proceedings of the United States
National Museum, 24(1246): 135–162.
Rogers DS, González MW. 2010. Phylogenetic relationships among spiny
pocket mice (Heteromys) inferred from mitochondrial and nuclear sequence
data. Journal of Mammalogy, 91(4): 914–930.
van Roosmalen MGM, van Roosmalen T, Mittermeier RA, Rylands AB.
2000. Two new species of marmoset, genus Callithrix erxleben, 1777
(Callitrichidae, Primates), from the Tapajós/Madeira interfluvium, South
Central Amazonia, Brazil. Neotropical Primates, 8: 2–18.
van Roosmalen MGM, Frenz L, van Hooft P, De Iongh HH, Leirs H. 2007. A
new species of living peccary (Mammalia: Tayassuidae) from the Brazilian
Amazon. Bonner Zoologische Beiträge, 55(2): 105–112.
Rosen DE. 1978. Vicariant patterns and historical explanation in
biogeography. Systematic Biology, 27(2): 159–188.
Simpson GG. 1961. Principles of Animal Taxonomy. New York: Columbia
University Press.
Solari S. 2004. A new species of Monodelphis (Didelphimorphia:
Didelphidae) from southeastern Peru. Mammalian Biology-Zeitschrift für
Säugetierkunde, 69(3): 145–152.
Tattersall I. 2007. Madagascar’s lemurs: cryptic diversity or taxonomic
inflation? Evolutionary Anthropology: Issues, News, and Reviews, 16(1):
12–23.
Tinbergen N. 1959. Behaviour, systematics, and natural selection. IBIS,
101(3–4): 318–330.
Tobias JA, Seddon N, Spottiswoode CN, Pilgrim JD, Fishpool LDC,
Collar NJ. 2010. Quantitative criteria for species delimitation. IBIS, 152(4):
724–746.
Tsang SM, Cirranello AL, Bates PJJ, Simmons NB. 2016. The roles of
taxonomy and systematics in bat conservation. In: Voigt CC, Kingston
T. Bats in the Anthropocene: Conservation of Bats in a Changing World.
Cham: Springer.
Thinh VN, Mootnick AR, Thanh VN, Nadler T, Roos C. 2010. A new species
of crested gibbon, from the central Annamite mountain range. Vietnamese
Journal of Primatology, 4: 1–12.
Van Valen L. 1976. Ecological species, multispecies, and oaks. Taxon,
25(2–3): 233–239.
Velazco PM, Gardner AL, Patterson BD. 2010. Systematics of the
Platyrrhinus helleri species complex (Chiroptera: Phyllostomidae), with
descriptions of two new species. Zoological Journal of the Linnean Society,
159(3): 785–812.
Voss RS, Hubbard C, Jansa SA. 2013. Phylogenetic relationships of New
World porcupines (Rodentia, Erethizontidae): implications for taxonomy,
morphological evolution, and biogeography. American Museum Novitates,
3769: 1–36.
Voss RS, Díaz-Nieto JF, Jansa SA. 2018. A revision of Philander
(Marsupialia: Didelphidae), Part 1: P. quica,P. canus, and a new species
from Amazonia. American Museum Novitates, 3891: 1–70.
Wheeler QD, Meier R. 2000. Species Concepts and Phylogenetic Theory:
A Debate. New York: Columbia University Press.
Wiens JJ, Servedio MR. 2000. Species delimitation in systematics: inferring
diagnostic differences between species. Proceedings of the Royal Society
B: Biological Sciences, 267(1444): 631–636.
Zachos FE. 2009. Gene trees and species trees–mutual influences and
interdependences of population genetics and systematics. Journal of
Zoological Systematics and Evolutionary Research, 47(3): 209–218.
Zachos FE, Apollonio M, Bärmann EV, Festa-Bianchet M, Göhlich U,
Habel JC, Haring E, Kruckenhauser L, Lovari S, McDevitt AD, Pertoldi
C, Rössner GE, Sánchez-Villagra MR, Scandura M, Suchentrunk F. 2013.
Species inflation and taxonomic artefacts—a critical comment on recent
trends in mammalian classification. Mammalian Biology-Zeitschrift für
Säugetierkunde, 78(1): 1–6.
Zachos FE. 2013. Species splitting puts conservation at risk. Nature,
494(7435): 35.
Zachos FE, Lovari S. 2013. Taxonomic inflation and the poverty of the
Phylogenetic Species Concept-a reply to Gippoliti and Groves. Hystrix,
24(2): 142–144.
Zachos FE. 2014a. Commentary on taxonomic inflation, species
delimitation and classification in Ruminantia. Zitteliana B, 32: 213–216.
Zachos FE. 2014b. Paraphyly—again!? A plea against the dissociation of
taxonomy and phylogenetics. Zootaxa, 3764(5): 594–596.
Zachos FE. 2015. Taxonomic inflation, the phylogenetic species concept
and lineages in the tree of life–a cautionary comment on species splitting.
Journal of Zoological Systematics and Evolutionary Research, 53(2):
180–184.
Zachos FE. 2016a. Species Concepts in Biology: Historical Development,
Theoretical Foundations and Practical Relevance. Cham: Springer.
Zachos FE. 2016b. Tree thinking and species delimitation: guidelines for
taxonomy and phylogenetic terminology. Mammalian Biology-Zeitschrift für
Säugetierkunde, 81(2): 185–188.
Zander RH. 2007. Paraphyly and the species concept, a reply to Ebach &
al. Taxon, 56(3), 642–644.
8www.zoores.ac.cn
