Evolutionary Anthropology 16:12–23 (2007)
ISSUES
Madagascar’s Lemurs: Cryptic Diversity or
Taxonomic Inflation?
IAN TATTERSALL
We live in inflationary times. A quarter of a century ago, cigarettes were about
$1 a pack in New York City, a bottle of Château Beaucastel set you back $15,
and there were 36 different species of lemur alive in Madagascar1 (Table 1).
Today the equivalent figures are $7.40, $95, and 83 lemur species2 (Table 1).
The increase in dollar prices has a lot to do with the economics of growth,
something that obviously cannot be sustained indefinitely on a finite planet. Is
the recent inflation in lemur taxonomy any more secure? The question is all the
more worth asking because this is no isolated phenomenon: Madagascar’s primates have not been alone in multiplying. The same burgeoning of species
names has occurred throughout the order Primates3,4 and beyond,5 provoking
both concern and energetic debate.6–9 Interestingly, this debate has largely
unfolded among ecologists, conservationists, and other ‘‘consumers’’ of taxonomy; many ‘‘producers’’ seem to be content to generate new taxonomies with a
remarkable lack of introspection, as if they were no more than passive consequences of more lofty concerns. And because the same causes underlie taxonomic inflation in Madagascar as elsewhere, this extraordinary island once again
presents us with a microcosm of the larger world.
According to Mittermeier and colleagues,2 at the early 2006 level Madagascar is home to 11% of all primate
species and subspecies, and fully 21%
of all primate genera. Even if one or
both of these figures is inflated, nobody
questions that the primate diversity that
still survives on the island is extraordinary. Interestingly, the recognized
generic abundance has only modestly
increased; it is overwhelmingly the promotion or re-promotion of subspecies
Ian Tattersall is a curator in the Division
of Anthropology of the American Museum of Natural History, New York City.
He is most recently the author, with Rob
DeSalle, of Human Origins: What Bones
and Genomes Tell Us About Ourselves.
E-mail address: [email protected]
Key words: Madagascar; lemurs; species; diversity; systematics
C 2007 Wiley-Liss, Inc.
V
DOI 10.1002/evan.20126
Published online in Wiley InterScience
(www.interscience.wiley.com).
to species, or the recognition of new
cryptic species among the nocturnal
forms, that has led to the recent enormous increase in apparent lemur diversity. Since 1982 we haven’t discovered
many new populations of lemurs in
Madagascar, and we’ve found rather little that looks distinctly different to the
eye from what we knew before. So why
the systematic explosion? Well, what
has dramatically changed since my
1982 survey is our operating assumptions about what species are and how
we recognize them. That is why this survey of lemur species begins with a look
at how we might best distinguish species in a fauna such as Madagascar’s.
WHAT DO WE MEAN BY SPECIES?
Species are the basic units into which
groups of individuals are ‘‘packaged.’’
But Nature is not necessarily neatly
packaged, as witness the multitude of
species definitions currently on offer:
Coyne and Orr10 recently counted a
minimum of 25. Leaving aside the con-
cerns of paleontologists, who have their
own unique set of woes, since around
the middle of the twentieth century the
species definition to beat has been
Ernst Mayr’s biological species concept, which, in its latest restatement,
characterizes species as ‘‘groups of
interbreeding natural populations that
are reproductively isolated from other
such groups.’’ Emphasizing as it does
the isolating mechanisms that keep
populations apart, this is clearly an
exclusionary definition. The opposite
approach is, predictably enough, inclusionary, emphasizing reproductive cohesion within populations. Probably
the best-known formulation of this kind
is Paterson’s recognition species concept, which defines a species as ‘‘that
most inclusive population of individual
biparental organisms which shares a
common fertilization system.’’ A third
major category of species definitions is
evolutionary, placing the emphasis on
ancestry, diagnosability and, in some
cases, genetic coalescence. Although
the original evolutionary species concept is attributed to Simpson,13 the
most influential definition of this kind
is Cracraft’s14 initial formulation of the
phylogenetic species concept (PSC).
According to Cracraft, a phylogenetic
species is an ‘‘irreducible (basal) cluster
of organisms that is diagnosably distinct from other such clusters, and
within which there is a paternal pattern
of ancestry and descent.’’ More recent
variations of the PSC have unfortunately tended to focus simply on diagnosability.
Each of these categories of species
definition, like the individual definitions
themselves, suggests a different operational approach to the practical matter
of recognizing species in Nature. Each
ISSUES
Madagascar’s Lemurs 13
TABLE 1. Mittermeier et al. (2006)2
Classification of the Malagasy Lemurs,
Annotated to Show Contrasts with
Tattersall (1982)1 Classification Plus
Recent Additions.
Family Cheirogaleidae
Genus Microcebus1
M. murinus*
M. rufus*
M. berthae
M. myoxinus
M. griseorufus
M. ravelobensis
M. sambiranensis
M. tavaratra
M. lehilahytsara
M. jollyae1
M. mittermeieri1
M. simmonsi1
M. mamiratra2
Genus Allocebus
A. trichotis*
Genus Mirza
M. coquereli*
M. zaza
Genus Cheirogaleus
C. major*
C. medius*
C. crossleyi
C. adipicaudatus
C. minusculus
C. ravus
C. sibreei
Genus Phaner
P. furcifer*
P. electromontis
P. pallescens
P. parienti
Family Lepilemuridae
Genus Lepilemur
L. mustelinus*
L. microdon
L. leucopus**
L. ruficaudatus**
L. edwardsi**
L. dorsalis**
L. ankaranensis
L. septentrionalis
L. aeeclis2
L. randrianasoli2
L. sahamalazensis2
L. ahmansoni3
L. betsileo3
L. fleuretae3
L. grewcocki3
L. hubbardi3
L. jamesi3
L. milanoii3
L. petteri3
L. seali3
L. tymerlachsoni3
L. wrighti3
L. mittermeieri4
TABLE 1. (Continued).
Family Lemuridae
Genus Hapalemur
H. griseus*
H. aureus
H. occidentalis**
H. alaotrensis**
H. meridionalis
y
Genus Prolemur
P. simus*
Genus Lemur
L. catta*
Genus Eulemury
E. fulvus*
E. rufus**
E. albifrons**
E. sanfordi**
E. collaris**
E. albocollaris**
E. macaco*5
E. rubriventer*
E. coronatus*
E. mongoz*
Genus Varecia
V. variegata*6
V. rubra**
Family Indriidae
Genus Avahi
A. laniger*
A. occidentalis**
A. unicolor
A. cleesei
Genus Propithecus
P. verreauxi*
P. deckeni**
P. coronatus**
P. coquereli**
P. tattersalli
P. diadema*
P. edwardsi**
P. candidus**
P. perrieri**
Genus Indri
I. indri*
Family Daubentoniidae
Genus Daubentonia
D. madagascariensis
* Species recognized in Tattersall 1982.1
** Recognized as subspecies in Tattersall
1982.1
y
Genus not recognized in Tattersall
1982.1
1
Species added by Andriaholinirina
et al. in 2006.40
2
Species added by Louis et al. 2006.27
3
Species added by Louis et al. in
2006.42
4
Species added by Rabarivola et al.43
5
Species monotypic in Tattersall 1982,1
contains two subspecies in Mittermeier
et al. 2006.2
6
Species monotypic in Tattersall 1982,1
contains three subspecies in Mittermeier et al. 2006.2
is posed within the context of a particular set of problems faced by the systematist and each presents its own peculiar
difficulties. How do we choose between
them? Brookfield15 took a down-toearth point of view, noting that while
species definitions abounded, no imaginable set of experiments could resolve
the choice between them. The corresponding advice was to ‘‘settle on our
favorite definition, use it, and get on
with the science.’’ But even this common-sense exhortation carries its own
difficulties. For if we all choose a different definition of what species should
be, then we will all be doing different
science, and neither our terminologies
nor our results will necessarily be comparable.
Probably the chief reason for this
existential mess is that species are most
fundamentally the products of speciation; and while speciation is something
that we tend to think of as a unitary
mechanism, it may, in fact, result from
a whole raft of different causes, from
point mutations through karyotypic
and morphological rearrangements all
the way up to behavioral factors.16 The
only thing these mechanisms need have
in common is that they give rise to historically individuated entities (see Ghiselin17 for a discussion of the ‘‘speciesas-individuals’’ notion), among which
the possibility of reticulate evolutionary
patterns is ended. In a sense, of course,
this brings us back to reproductive isolation. But complicating the matter is
the fact that among primates historical
individuality may apparently be achieved even without total rupture of
breeding behaviors. A few observations
of mating, or even of apparently undisadvantaged hybrid formation, would
not be enough to demonstrate that two
parapatric differentiated populations
belong to the same species; the only
way of doing this would involve the normally Herculean task of showing that
the gene pools of those populations are
actively in the process of reintegrating
after geographical separation.
In any event, while nature is clearly
‘‘packaged’’ at some biologically significant level, at the finest degree of detail it
is, at best, untidily packaged. Perhaps it
is unrealistic to expect the reductionist
human mind-set to be happy with the
resulting blurry lines, but the messy
reality seems inescapable, especially
ISSUES
14 Tattersall
given that there is no necessary relationship between speciation and morphological change.18 Indeed, it is this
lack of association that constitutes the
major weakness in phylogenetic species
concepts, especially the more fundamentalist versions which, in making
species minimal diagnosable units,
ignore the undeniable reality of fairly
frequent within-species polytypism. No
matter how innovative it may be genetically or morphologically, no population
faces a future as an independent evolutionary entity until it is ‘‘validated’’ by
speciation, an event that seems best
defined simply as the biological means
by which an historically individuated
lineage becomes established. The riotous diversity of life ultimately depends
on the combination of the twin, but often unrelated, processes of differentiation and speciation. We should not be
misled by the fact that most of the time
local diversification seems to work
within what, to misappropriate a term
from Eldredge,19 one might call a
‘‘sloshing bucket’’ principle, whereby
both genetic and phenotypic frequencies move back and forth within the
containing wall of the species, the occasional overflow being largely or entirely
lost.
What does this mean for defining species or, more to the point for the working systematist, for recognizing them in
living biotas? If the species we see
around us have originated in events of
many different kinds, it seems hardly
realistic for us to seek a one-size-fits-all
definition of this most basic of biological units. But maybe there is still hope.
If species, however formed, are indeed
individuals,17 perhaps systematists can
usefully see species in somewhat the
same light that judges see pornography,
which they claim to recognize operationally even if they can’t define it.
Determinations are made case by case,
weighing all of the facts and circumstances, whatever they may be. It seems
entirely reasonable to transpose this
approach to the biology of living populations, even though it means abandoning the notion of the silver bullet in species recognition. Instead we have to
weigh all the evidence bearing on
whether a particular group is indeed
historically individuated; that is, not at
either potential or actual risk of being
reabsorbed into its parent population.
Among close relatives, this is manifestly
a judgement call on a matter that will,
even in principle, only ever be demonstrable in hindsight. Not all decisions
will be clear-cut. However, such decisions will have the advantage of incorporating multiple aspects of population
biology. In this perspective, a handful
of DNA base substitutions may not by
themselves give reason for recognizing
a species unit, any more than a few
instances of hybridization may be
grounds for denying one. The crucial
element is the probability of individuation.
LEMUR SPECIES
My 1982 genus- and species-level
classification of the Malagasy primates1
represented more or less a consensus
view for the time (compare with Petter,
Albignac, and Rumpler20). This consensus had existed in its broad outlines
since the minimalist Ernst Schwarz
reviewed the lemur fauna in 193121 and
was still accepted in its essentials in the
mid-1990s when the first edition of
the Mittermeier et al. field guide to the
lemurs22 appeared.
Apart from species described in
the quarter-century between 1982 and
2006, the most striking difference
between my 1982 classification1 and
that provided by Mittermeier et al.2 in
their second edition of 2006 is that the
former included several strongly polytypic lemur species, namely Phaner furcifer, Lemur fulvus, Varecia variegata,
Lepilemur mustelinus, Hapalemur griseus, Avahi laniger, Propithecus diadema, and Propithecus verreauxi. In the
Mittermeier et al. 2006 classification,2
there are only two polytypic lemur species, Varecia variegata and Lemur macaco, and even these are polytypic only
because they contain subspecies that
did not even exist in my 1982 classification. Otherwise, in the new classification lemur species remain rigorously
monotypic. More than half of the species-level diversity added between 1982
and 2006 consists of the promotion of
subspecies to species. With the exception of the large-bodied and diurnal Propithecus tattersalli, the balance is
accounted for by the description of new
species or the resurrection of old ones
belonging to the nocturnal, smaller-bodied, and more discreetly colored portion
of the lemur fauna. On the face of it, the
recognition of some new species in the
latter category does not seem altogether
surprising, but one might equally wonder just how probable it is that, among
a fauna as diverse as Madagascar’s primates, long established on a large and
environmentally varied land mass, there
should be almost no polytypic species.
This is why I will now look at the newly
recognized lemur species case-by-case
in an attempt to assess the foundations
for the recent apparent explosion in
lemur species diversity.
Family Cheirogaleidae
The recent multiplication of lemur
species has been most rampant among
the nocturnal mouse and dwarf lemurs,
family Cheirogaleidae. Traditionally,
the number of new species described
was kept relatively low by typically
cryptic variation in external morphological characters and coloration, and
was mostly driven by discovery or reinterpretation of old illustrations. In the
genus Microcebus, the recent dramatic
increase in the number of species recognized has been largely due to molecular
findings, while the multiplication of
Cheirogaleus species is principally due
to reevaluation of mostly ancient museum specimens.
Genus Cheirogaleus
Since 1982, the dwarf lemur genus
has swelled from two species, the western Cheirogaleus medius and the larger
eastern C. major,1 to seven.2 The additions all stem from a restudy of museum specimens by Groves,23 who recognized two groups within Cheirogaleus. One group contained C. medius
and C. adipicaudatus, while the other
embraced C. major plus the revived C.
crossleyi and C. sibreei, and the two new
species C. ravus and C. minisculus.
From the beginning the nomenclature
of Cheirogaleus species and populations
has been a systematist’s nightmare, but
there can be little doubt of the accuracy
of Groves’ perception of greater diversity among the dwarf lemurs than traditionally has been acknowledged. How
to classify it is another question. The
basic distinction between C. major and
C. medius seems to stand, but there is
ISSUES
more variety and complexity of distribution within each group than monotypy for each implies. Hapke and colleagues24 additionally reported observing three distinctive dwarf lemur
morphs near Fort-Dauphin in the far
southeast; two they identified as C.
major and C. medius, and the third they
assigned to C. crossleyi, a form otherwise reported only from the north. The
visual distinctiveness of the three
morphs was corroborated by metrics
and molecular analyses.
Clearly, there are more species of
Cheirogaleus than the two traditionally
recognized, but sorting out this variety
is bedevilled by our ignorance of the geographic and morphological boundaries of the variants involved. Field observations are few and mostly anecdotal; it
is possible that pelage colorations vary
seasonally as well as geographically (J.
Masters, personal communication);
museum collections are sparse; and reliable locality information is rarer yet. In
some cases there is substantial reason
to believe that distinctive forms of Cheirogaleus are indeed sympatric,25 suggesting species-level differentiation, but
exactly which taxa are involved is still a
matter of speculation. Groves’ revision
of the dwarf lemurs is certainly a necessary foundation on which to refine our
classification on the basis of future field
and molecular observations. However,
while the earlier two-species division
certainly understates dwarf lemur diversity, formal revision of Cheirogaleus taxonomy—beyond, perhaps, the additional recognition of a species that
might be called C. crossleyi—seems premature at this point.
Genus Microcebus
The mouse lemur genus Microcebus
accounts for much of the increase in
lemur species since 1982, at which time I
recognized two species, the gray, largeeared western M. murinus and the reddish-brown, small-eared, mostly eastern
M. rufus.1 The most recent counts2,26,27
yield the thirteen species listed in Table 1
and hint at more to come.
The first augmentation came with the
resurrection by Schmid and Kappeler28
of the species name M. myoxinus Peters
for a long-rumored rufous form living
in sympatry with the gray, longer-eared
Madagascar’s Lemurs 15
M. murinus at Kirindy in western
Madagascar. Subsequently, Zimmermann et al.29 created the new species M.
ravelobensis to contain a golden-brown
form living sympatrically with gray
mouse lemurs in the Ankarafantsika
forest of the northwest. External morphometrics suggested that the new species was also distinct in body proportions both from the sympatric gray
mouse lemurs and the rufous mouse
lemurs of Kirindy and Andasibé in the
east. The authors also found that at
Ampijoroa the two kinds of mouse
lemur showed overlapping yet distinct
habitat preferences. Shortly thereafter,
Rasoloarison et al.,30 studied craniodental and external characters in newly
acquired samples of mouse lemurs from
a dozen localities in western Madagascar, including Kirindy and Ampijoroa.
These new specimens confirmed the
distinctness of the rufous Kirindy and
Ampijoroa populations. However, Rasoloarison, et al.30 concluded that the
name M. myoxinus should properly
apply to yet another distinct mouse
lemur population, the type locality of
which is to the south of Kirindy, and
proposed to call the Kirindy form M.
berthae. They also resurrected the name
M. griseorufus Kollman for a population
sampled near Beza Mahafaly in the
southwest and judged that other populations from the Ankarana Massif in the
north of Madagascar and the Sambirano in the northwest additionally merited recognition as distinct species, giving them, respectively, the names M.
tavaratra and M. sambiranensis.
With multiple samples for each population at hand, Rasoloarison, et al.30
cited substantial distinctions in metrics,
coloration, and external proportions in
support of each of their named units.
Four of their recognized species, M.
tavaratra, M. sambiranensis, M. ravelobensis, and M. berthae, were reported
only from a single locality or from
closely grouped localities, while the
others, based on the data presented by
Rasoloarison, et al.30 and by Yoder
et al.31 have wider distributions. M. murinus occurs from Berenty in the far
south, potentially as far north as the
Sambirano, and more certainly to Kirindy; M. griseorufus from Berenty north
and west toward Morombe; and M.
myoxinus from the Tsiribihina River
north, possibly as far as Soalala. M. mur-
inus is recorded in sympatry with M.
berthae at Kirindy, with M. griseorufus at
Beza Mahafaly and Berenty (where they
are ecologically differentiated32), and
probably with M. ravelobensis in the
Ankarafantsika. M. tavaratra and M.
sambiranensis reportedly occur alone,
while on the grounds of probable distribution it seems likely that M. myoxinus
also occurs alongside M. murinus.
All of these distributions are based on
highly incomplete information that necessarily yields a very provisional set of
biological units. Nonetheless, Yoder
et al.31,32 have reported molecular evidence supporting the notion that all of
the species recognized by Rasoloarison,
et al.30 represent reproductively isolated
entities.
Rambinintsoa et al.26 additionally
described mouse lemurs on the island
of Nosy Bé in the northwest as a new
species, M. mamiratra. This was, however, diagnosed strictly on the inadequate basis of mtDNA distance (see
later discussion of Lepilemur).
In eastern Madagascar, a similar scenario appears to be developing. No morphological study comparable to that of
Rasoloarison, et al.30 has been undertaken in this huge region, formerly
thought to be populated throughout by
the single species M. rufus. However, in
2005 Kappeler et al.33 reported the discovery at Andasibé and Mantadia, north
of Moramanga, of very small-bodied
mouse lemurs boasting short ‘‘bright
maroon’’ fur with orange tinges and a
characteristic variant of the mitochondrial cytochrome b gene. Noting the distinctiveness of this population on both
the morphological and molecular levels,
they named this form M. lehilahytsara.
Given that M. rufus also is well documented to occur in this region, this
seems a reasonable move pending further information.
Louis et al.27 followed with a survey
based on samples freshly collected at a
dozen sites in the eastern region. Analyses of a variety of mitochondrial markers
led Louis et al.27 to redefine M. rufus
(naming a topotype from Ranomafana
National Park, east of Fianarantsoa),
which they recognized only from relatively high-altitude populations known
at Ranomafana and Mantadia. At the
same time they named three new species, each one distinctive not only at the
molecular level, but in pelage and exter-
ISSUES
16 Tattersall
nal characteristics: M. mittermeieri,
known from the Anjoharibé-Sud Special Reserve in the northeast; M. jollyae,
from Mananjary and Kianjavato, east of
Ranomafana and at lower elevations;
and M. simmonsi, from Betampona
Special Reserve and Zahamena National Park, to the north of Tamatave.
This still leaves vast tracts of what was
formerly M. rufus territory unsurveyed.
What does all this mean in terms of
Microcebus diversity? At the minimum,
this diversity appears hugely underestimated by recognizing only two monotypic species within the genus. Tiny size,
cryptic coloration, and nocturnal habits
have been allowed to obscure real biological variety. But at what taxonomic
level(s) this diversity should be recognized is another matter. There is plenty
of evidence of differentiation among
mouse lemur populations at levels ranging from the molecular to pelage and
external characters, craniodental structure, and ecological preference. But
whether the units recognized are definitively individuated historical entities, or
even discontinuous ones, is not known
in all cases. The apparent sympatry of
M. murinus with such taxa as M. ravelobensis, M. berthae, and M. myoxinus,
along with ecological indicators, is good
evidence that the first of these at least is
specifically distinct from the others. The
same can apparently be said for M. rufus
and M. lehilahytsara. But what of M. jollyae, M. simmonsi, M. mittermeieri, M.
rufus, and M. mamiratra, which might,
on the basis of recorded localities, be
viewed as local intraspecific variants?
This conclusion would be hard to square
in detail with the phylograms presented
by Louis et al.27, but the quantitative
analyses are not inordinately robust.
Moreover, the fact that the question can
be legitimately asked is a good indication that we will need to know a great
deal more about the mouse lemurs
before we can derive anything approaching a definitive account of the
hierarchy of diversity in Microcebus, a
point that Louis et al.27 emphasize.
Nonetheless, at least a significant part of
the recent increase in mouse lemur species seems justified by available facts.
Genus Mirza
In 2005, Kappeler et al.33 proposed
that the two disjunct isolates of Mirza
coquereli should be separated at the species level, citing morphometric, molecular, and behavioral differences, including substantial disparity in the timing
of reproductive activity. The type locality of M. coquereli being Morondava in
the central-west, these authors proposed the new name M. zaza for the far
northwestern population. The differences Kappeler et al. described are substantial, and certainly warrant the recognition of two taxa. External differences between the two are on the order of
those separating sympatric mouse
lemur species, but the reported genetic
distance (3.3%–3.5%) in the cytochrome b gene is fairly modest. Still,
given that breeding seasons are fully
out of synchrony, provisional acceptance of two species seems justified.
Genus Phaner
The poorly known fork-marked
lemurs exist in a series of isolates dotted
around the periphery of Madagascar.
Until 1991, the single species Phaner
furcifer was considered monotypic, but
at that time Groves and I,34 working
with museum specimens, pointed out
substantial variations in size, pelage,
and body proportions among the various isolates. We proposed dividing the
known populations into four separate
subspecies, hinting that fuller surveys
would reveal yet more. In 2001, Groves
raised these four subspecies of P. furcifer to the rank of species35 (Table 1), but
gave no reason other than their discreteness as already described. If the
notion of subspecies means anything at
all, it recognizes that local populations
of the same species are likely to differ
from one another in precisely the kinds
of characteristics that Groves and I initially pointed out. If this is the case,
then simple discreteness is not, in and
of itself, an adequate criterion for species recognition. In this case, the balance of inadequate available information tips away from species distinction.
Family Lepilemuridae
This family contains the single living
genus Lepilemur, which has a particularly tortuous recent taxonomic history.
Reduced in 196036 to a single species
with five subspecies, by 1977 the genus
had seven species, one with four subspecies.20 In 19821 it was back down to
one species, with six subspecies distributed around the entire periphery of
Madagascar. Since then it has undergone a dramatic re-expansion (Fig. 1).
Genus Lepilemur
These medium-to-small-bodied lemurs
are nocturnal and exhibit the subtle differences in pelage coloration among
local variants that are typical of nocturnal forms. Recent systematic contributions, for example by Ishak, et al.,37
have tended to build on the 1977 classification20 with its seven species, only
one polytypic. Since the early 1970s,
most of these species have been characterized karyotypically as well as by visual features, and all are, as far as is
known, distributed discretely around
the periphery of Madagascar.
In 2001, Rumpler et al.38 concluded
that the most northerly Lepilemur species, L. septentrionalis, already known
to be karyotypically polymorphic, consisted of two reproductively incompatible but externally cryptic populations,
both karyotypically heteromorphic and
each with a distinctive mtDNA (cytochrome b) signature. One of the original
subspecies populations, confined to the
Sahafary forest to the east of the Montagne d’Ambre, was raised to species
level as L. andrafiamenensis. However,
to judge from the discussion by Ravoarimanana et al.,39 who subsequently
affirmed the hypothesis of cryptic speciation in northern Lepilemur, the name
for this species, possibly now extinct,
should probably be L. sahafarensis. The
remaining northern populations, formerly grouped into three subspecies,
were lumped into a monotypic L. septentrionalis. With the subsequent report
by Andriaholinirina et al.,40 all eight
species of Lepilemur thus recognized
were characterized on karyotypic
grounds.
Andriaholinirina et al.,40 have recently published the results of a study
of 99 Lepilemur individuals analyzed
for karyotype and 68 analyzed for the
complete mitochondrial cytochrome b
gene. Most major forested areas of
Madagascar north of about 218S latitude were represented, as well as the
ranges of all eight recognized Lepilemur
species except L. leucopus. Karyotypic
ISSUES
Figure 1. The diversity of Lepilemur species. Drawing by S. Nash. [Color figure can be
viewed in the online issue, which is available at www.interscience.wiley.com.]
Madagascar’s Lemurs 17
results generally supported the eightspecies division, while elevated specieslevel diversity was also suggested by the
generally high numbers of intergeneric
base substitutions noted in the cytochrome b gene compared to those
reported for other lemurs. Indeed,
based on the magnitude and patterns
of cytochrome b resemblance derived,
Andriaholinirina et al.40 proposed three
new species, L. aeeclis, L. randrianasoli,
and L. sahamalazensis, to contain, respectively, Lepilemur populations from
east of the Mahavavy-Sud River estuary, around Bemaraha, and the Sahamalaza Peninsula. The first two of
these sites fall within the range of L.
ruficaudatus as redefined by Zaramody
et al.,41 and the third within that of
L. dorsalis.
Soon after the appearance of the
article by Andriaholinirina et al.,40 a
stunning eleven additional Lepilemur
species, from widely scattered parts of
Madagascar but individually sampled
at closely grouped localities, and none
sympatric with any other sportive
lemurs (except possibly in the far
north), were reported by Louis et al.42
All eleven were diagnosed exclusively
on the basis of mtDNA (D-loop, PAST,
12s RNA) distances from their geographical neighbors or their apparent
closest relatives. Reported genetic distances between population pairs vary
from 1.0% to 16.9% and are clearly insignificant systematically at the lower
end of this range, though they are
highly suggestive when they approach
the upper limit. External and metric
descriptions accompanying the species
diagnoses were clearly made secondarily to identification on geographical
and molecular grounds. Finally (probably not the best word to choose),
Rabarivola et al.,43 created a new species, Lepilemur mittermeieri, for the
sportive lemur population on the
Ampasindava Peninsula. This species
was defined on karyotypic as well as
mtDNA criteria.
Although widely distributed and generally not hard to find, Lepilemur is
among the least-known of the lemurs.
Geographical barriers, principally rivers, are believed broadly to demarcate
the eight traditionally accepted Lepilemur taxa, but exact distributions are
unknown as, for the most part, is the
probable extent of within-population
ISSUES
18 Tattersall
variation in both external and molecular characteristics, let alone in behaviors. Mittermeier et al.2 allude to
reports of hybridization between L.
mustelinus and the very similar L.
microdon (lumped in 19821), but all
such information is anecdotal at best.
All that can be said with certainty is that
there is variation within Lepilemur and
that much of this variation appears to
be organized geographically. On the basis of the karyotypic and hybrid-recognition studies of Rumpler and his colleagues38–40 it seems reasonable that
most of the eight ‘‘core’’ taxa should
provisionally be recognized at the species level. On the other hand, even quite
large divergences in the cytochrome b
gene seem to constitute rather weak evidence for speciation in the case of the
three recently named species embedded
within the ranges of L. ruficaudatus and
L. dorsalis. Given that the karyotypes of
L. aeeclis and and L. randrianasoli are
the same as that of L. ruficaudatus, that
the pelages of L. aeeclis and L. sahamalazensis are described as ‘‘variable’’, and
that no external description at all is
given for the single-locality L. randrianasoli, it seems a little premature to
characterize these populations as species or, indeed, given their embedded
distributions, as subspecies. A stronger
argument can be made for Rabarivola
et al.’s43 L. mittermeieri and, perhaps
also, for Louis et al.’s42 karyotypically
distinctive L. jamesi from Manombo (Y.
Rumpler, personal communication).
While there is significant species-level
diversity in Lepilemur, it thus seems
probable that Andriaholinirina et al.’s40
count of eleven overstates what can be
justified on the basis of current information. Further, the additional species
reported by Louis et al.,42 all diagnosed
exclusively on genetic distance and all
allopatric, must be treated with extreme
caution until supporting data are forthcoming. By their nature, species diagnoses must be differential and based on
recognizable characters. Since distances are not discrete characters and,
indeed, different sequences can yield
identical distances, they are not in isolation appropriate for species diagnosis.
And even if they were, there is clearly
no percentage difference in sequence
for any mtDNA marker that infallibly
indicates species-level differentiation.
Indeed, the same populations may ex-
hibit significant differences in genetic
distance, according to the marker chosen.
As perhaps the most widely distributed in Madagascar of all lemur genera,
Lepilemur clearly shows an expected
high degree of local population differentiation. But of the 24 putative species
on offer as this goes to press, not many
more than a third can be accepted as
fully individuated on current evidence.
Family Lemuridae
In 1982, three genera were generally
recognized in the family Lemuridae:
Lemur, Varecia, and Hapalemur. Mittermeier et al.’s42 count in 2006 is five,
with the addition of the genera Eulemur, obtained by splitting the nominate
species Lemur catta from its former
congeners, and Prolemur, a result of
reseparating the greater bamboo lemur
from Hapalemur. Whether the first of
these splits is justified is a contentious
issue that is fortunately beyond my
scope here. What is germane is the multiplication of species that has occurred
within the genera Eulemur, Varecia,
and Hapalemur.
Genus Hapalemur
The 1982 classification of the principally diurnal Hapalemur recognized the
two living species H. simus and H. griseus, the latter with three karyotypically
distinct subspecies.44 A fourth subspecies, H. g. meridionalis, was added in
1987.45 During the 1980s, surveys at
Ranomafana and other sites in the
southeastern rain forest found H. simus
flourishing sympatrically not only with
H. griseus griseus, but with a distinctive
third species, H. aureus.46 Further allopatric subspecific variants of H. griseus
were later mooted, but not formally
named.47,48 In 2001, Groves35 returned
H. simus to the genus Prolemur in
which it had originally been described
and, without providing any rationale,
raised the former subspecies H. g. griseus, H. g. occidentalis, and H. g. alaotrensis to distinct species. Shortly thereafter, Fausser et al.,49 did the same with
the former H. g. meridionalis, while
again demoting the others to subspecies
of H. griseus. In 2006, Mittermeier
et al.2 recognized all the named taxa as
species in their own right. None of the
taxa formerly allocated to H. griseus
exist in sympatry and, while on grounds
of genetic distance Fausser et al.49
regard meridionalis as the outlier in that
clade, it is hard to make a clear-cut case
for definitive genetic separation within
the group. Given the extensive mutual
resemblances, morphological and molecular, of all of the forms traditionally
allocated to H. griseus, as well as their
contrasts with H. aureus, it seems premature at this point to do anything
more than recognize a single polytypic
species for these forms. While simus is
clearly the outgroup to the griseusþ
aureus clade, given the strong Gestalt
resemblances among all the gentle
lemurs it seems superfluous to place
this form in a separate genus.
Genus Eulemur
This cathemeral genus was named in
1988 by Simons and Rumpler50 to contain the five species of ‘‘true’’ lemurs
orphaned after Lemur catta was hived
off. All had long been seen as monotypic except for the famously polytypic
Eulemur fulvus, within which seven
subspecies were recognized. One of
these, E. f. mayottensis, was ultimately
absorbed into E. f. fulvus as an introduced insular isolate.22,51 In 1985, the
rediscovery of the blue-eyed lemur52
added a second polytypic species, E.
macaco, to the genus, but as a trend this
did not last long. In his primate classification of 2001, Groves35 recognized two
subspecies within E. macaco but, for
reasons unexplained, promoted every
one of the six subspecies of E. fulvus to
separate species status. Groves also
added one more for good measure,
based on two skins from near Farafangana that might be what Milne
Edwards and Grandidier75 had illustrated in 1890 as ‘‘Lemur mongoz var.
cinereiceps.’’ This was a bold move,
since museum collections everywhere
are well provided with skins, provenanced or otherwise, that cannot comfortably be squeezed into neat conceptions of the various E. fulvus subspecies. And it proved, just, too bold even
for Mittermeier et al.,2 who otherwise
followed Groves in recognizing the
other brown lemur variants as full species. Meanwhile, the IUSN/SSC Conser-
ISSUES
vation Breeding Specialist Group had
decided2 that full species status be
granted to the former E. f. collaris, E. f.
albocollaris, and E. f. sanfordi, while
maintaining E. f. fulvus, E. f. rufus, and
E. f. albifrons as brown lemur subspecies.
There is thus no question that there
is diversity in the Eulemur genus.
Everyone seems to be comfortable
with recognizing E. mongoz, E. coronatus, and E. rubriventer as monotypic species and E. macaco as a polytypic species with two subspecies.
The problem comes with the variants
that were formerly all viewed as subspecies of E. fulvus, in each of which
at least one sex is distinctive in pelage
pattern (Fig. 2). (Although, as noted,
museum specimens, as well as individuals observed in the field, are not
always easy to classify). Echoing an
earlier finding based on craniodental
characteristics,53 Wyner et al.54 used
the analysis of three mtDNA regions
to determine that the entire E. fulvus
complex formed a single clade, a conclusion later supported by Yoder and
Irwin.55 Wyner et al.54 further combined phylogenetic and gene-flow
analysis to reach the conclusion that
the parapatric albocollaris and collaris populations (which, despite the
fact that the females are virtually
indistinguishable, are karyotypically
very different, and do not produce
fertile offspring56) should be separated at the species level both from
each other and from the other brown
lemurs. At the same time, they recognized a high degree of interfertility
among the remaining brown lemur
taxa and reckoned that all four are
best seen as subspecies of a single
species. In this they agreed with Djlelati et al.56 who reached the same
conclusion on the basis of chromosomal studies of hybrids. Awkwardly,
though, both collaris and albocollaris
are known to produce fertile offspring with other E. fulvus.57 What is
more, field studies58,59 have shown
that natural hybrid zones exist
between both collaris and albocollaris and rufus in the Andringitra
National Park. Add to this that the
various populations of brown lemur
are distributed in an almost complete
ring around Madagascar, but not in a
neat succession—fulvus and rufus,
Madagascar’s Lemurs 19
Figure 2. The diversity of 4 species of Eulemur, formally included in the single species E. fulvus, now considered as separate species.
for example, are found on both east
and west coasts—and the historical
biogeography as well as the taxonomy of the group, poses something of
a conundrum.
Nonetheless, it is reasonably clear on
all criteria that the E. fulvus complex is
distinct from the other Eulemur species
and that the latter are, in turn, specifically distinct from each other. It also
seems a fairly firm conclusion that
the fulvus/albifrons/rufus/sanfordi forms,
while differentiated, are best regarded
as belonging to a single historical unit.
In other words, while all may be said to
represent potential new species, none
of them can yet be shown to have
speciated. The case for unity is less
clear-cut for the albocollaris and collaris forms. Probably nowhere will one
find a better example of the untidy
packaging of Nature. The forests of
Madagascar undoubtedly have more
surprises in store. Mittermeier et al.,2
for example, report a sighting of a single captive individual that remarkably
resembled Milne-Edwards and Grandidier’s ‘‘cinereiceps.’’ For the moment,
though, it appears that in species
terms the lower 1982 count is significantly closer to what can be justified
than the 2006 numbers.
Genus Varecia
My 1982 classification contained one
species of ruffed lemur, with two sub-
species (red-and-black and black and
white). Following Groves,26 the 2006
classification contains two species, one
with three subspecies. This result was
achieved by elevating the two subspecies to species and subdividing the
black-and-white form. Vasey and I60
recently reported the existence of a
hybrid zone between the red-and-black
and black-and-white forms north of
Maroantsetra, but noted that hybridization within the zone appears to be rare.
On this basis, it seems reasonable to
recognize two species. The black-andwhite form, which is distributed down
the east coast of Madagascar from Maroantsetra to Vangaindrano, shows a variety of pelage variants. However, it is
far from evident that these variants are
discretely distributed. Pending better
documentation, it seems premature to
recognize formal subspecies.
Family Indridae
Genus Avahi
For many years, the nocturnal woolly
lemurs of the eastern and western
regions of Madagascar were considered
subspecies of the single species Avahi
laniger. In 1990 Rumpler et al.61 plausibly separated the eastern and western
forms at the species level on karyotypic
grounds that suggested intersterility.
Subsequently, Thalmann and colleagues62,63 delimited three chromati-
ISSUES
20 Tattersall
cally distinct allopatric species in the
west. Mittermeier et al. accepted these
in their 2006 classification. Evidence of
specific separation is persuasive, if not
conclusive.
Genus Propithecus
Traditionally, two species of the diurnal sifakas were recognized, Propithecus diadema and P. verreauxi, respectively, with five and four subspecies. In
1988, Simons64 named an additional
karyotypically distinct species, P. tattersalli, which showed morphological
attributes of both the others as well as
external features of its own. Using
highly repeated DNA, Razafindraibe
et al.65 placed the new species as the
outgroup to P. verreauxi þ P. diadema.
In 1986 I reduced sifaka diversity by
synonymizing the two subspecies P. d.
edwardsi and P. d. holomelas, and by
suggesting that the same might be true
of P. v. coronatus and P. v. deckeni.66
Groves35 subsequently moved in the opposite direction, elevating the former P.
d. edwardsi and P. d. perrieri to full species and recognizing two subspecies
within P. diadema. He also promoted
the former P. v. verreauxi, P. v. coquereli, and P. v. deckenii to full species, with
the latter embracing the subspecies P.
d. deckenii and P. d. coronatus. Pastorini, et al.67 then used mtDNA distances
to restore the traditional two-species division, to suggest that the karyotypically
distinct P. tattersalli paired with P. v.
coquereli, and to conclude that subspecific distinction between P. v. coronatus
and P. v. deckenii is not warranted.
Thalmann et al.68 disagreed, presenting persuasive morphological and distributional evidence for distinguishing
P. v. coronatus from P. v. deckenii. They
also argued on morphological grounds
against the suggested synonymy of P.
tattersalli with P. v. coquereli. Mayor
et al.69 followed with molecular, cytogenetic, and morphological analyses that
suggested three clades within Propithecus: P. v. verreauxi; the four P. diadema
taxa; and P. tattersalli þ P. v. coquereli.
Their sample did not include P. v. coronatus/deckeni. Elevating all of the P. diadema subspecies to species level, Mayor
et al.69 recognized seven species among
those taxa sampled, albeit using a
highly restrictive variant of the PSC
Figure 3. The diversity and geographic distribution of Propithecus species. Drawing by
S. Nash. [Color figure can be viewed in the online issue, which is available at www.
interscience.wiley.com.]
based purely on diagnosability. Mittermeier et al.,2 using a ‘‘precautionary
principle,’’ adopted a similar schema,
with the addition of both P. deckenii
and P. coronatus, while noting the possibility that yet more Propithecus species remained unnamed.
Clearly, the ubiquitous diurnal genus
Propithecus is represented by several
distinctive variants in different parts of
Madagascar, each, on the whole, easily
recognizable by pelage pattern (Fig. 3).
The distributions of the diadema group
taxa appear to be more or less contiguous in the humid forests of the east
coast, with perrieri an outlier in the far
north. If deckenii and coronatus are
combined there is a broadly similar
pattern of distribution of the verreauxi
group in the west and south, while P.
tattersalli forms a tiny isolate in the
north. At the same time, there is considerable variation in pelage coloration
within many variants, perhaps most
famously P. d. diadema, which appears
to converge chromatically with P. d.
edwardsi at the southern limit of its
range.2,70 This by itself suggests an
imperfect demarcation between the
two taxa, implying clinal variation and
arguing against specific distinction. In
the west and south coronatus and deckenii may yield a similar geographic pattern. Particularly striking is the case of
the melanistic ‘‘majori’’ form occasionally observed within verreauxi. Given
such inconsistency and the fact that
most ranges are imperfectly surveyed,
dubbing each principal variant a species seems a little premature, especially
in view of the fact that many recent
studies relied on distance measures and
ISSUES
Madagascar’s Lemurs 21
diagnosability-based notions that effectively equate OTUs with species and
leave in abeyance the question of historical individuation.
DISCUSSION
From this brief review two major
points should be evident: first that there
is a great deal of geographically organized variety among the lemurs; and secondly that how one organizes that variety depends largely on one’s concept of
species. The recent multiplication of
lemur species is partly due to new discoveries and better information about
lemur distributions and population
characteristics. But it is to a far greater
extent due to a shift toward fundamentalist notions of the phylogenetic species. These discard the nuances of Cracraft’s14 original definition in favor of
crude diagnosability; and if one accordingly equates species purely with minimal diagnosable units, then on current
evidence a good deal of the recent efflorescence of lemur species is justifiable.
However, diagnosability—the ability to
demonstrate some or indeed any difference—may well in many cases be as
much a matter of sampling error as of
discontinuity, especially in Madagascar’s badly fragmented and degraded
habitats. Invoking genetic distances as
substitutes for diagnostic features only
exacerbates this problem. What is
more, innovation in local populations
of the same species is the engine of evolutionary change and is independent of
speciation, as any member of Homo
sapiens can attest. Indeed, if every local
variant is a species, we rob microevolution of a place to occur.
To put it another way, if we go with
diagnosability there is a very large number of lemur species in Madagascar, all
monotypic. Is this plausible? The argument might be made that lemurs have
been so long in Madagascar, effectively
without competition, that before the
recent arrival of human beings the
island’s habitats were ‘‘saturated,’’ and
that the lemur fauna was essentially in
a long-term steady state. Several recent
biogeographic studies71–73 cast doubt
on this, and the recent ‘‘superimposition’’ of the Eulemur fulvus radiation
on the earlier one of Eulemur species is
a particularly compelling counterargu-
ment. What is more, local differentiation among populations of widely distributed species is a well-documented
general phenomenon, particularly in
tropical areas; indeed, it is subspecies,
diagnosable local variants, that underwrite the appearance of new species.
Since speciation is not an inevitable
passive result of morphological differentiation, we would expect to find
within-species diversity in any aggregation of habitats as diverse as Madagascar’s. That is, indeed, what we find, as
long as we resist arbitrarily defining all
of the variants we perceive as species
purely on the grounds of diagnosability
or genetic distance.
If diagnosability by itself is thus not
enough, and we have to add Ghiselin’s
element of historical individuation back
into the mix, then we need to base our
judgments about what is or is not a species on information that goes well
beyond pure morphology or genetic
structure. Such information includes
geographical distributions, ecological
displacements, potential reproductive
impediments of all kinds, the nature of
any hybrid zones, and so forth. Sadly,
in the case of many lemurs we have to
make our inferences about individuation using sketchy data that provide a
highly suboptimal basis for ‘‘balance of
the evidence’’ evaluations. Given the
rapid disappearance of lemur habitat in
Madagascar, much of the necessary information may never be available. What
is more, while legal disputes about pornography are adjudicated in the courtroom, we have no court-equivalent in
zoology. All we have is a crowd of often
vociferous advocates. Based on the evidence already reviewed, however, it
seems safe to conclude that while some
of the recent proliferation in lemur
species names is justified, most is not,
at least on the evidence we now have.
Certainly, there is more (even much
more) species-level diversity among
the lemurs of Madagascar than we can
convincingly characterize at present.
But on the information now available, it is hard to justify formal recognition of more than about 47 or 48
living lemur species and a total of
around 62 taxa including subspecies.
This is a substantial increase over the
36 species I recognized in 1982, but a
much lower figure than the 84 that a
naı̈ve reading of the recent literature
would suggest. On the other hand,
this last number may be a rough
guide to the minimum number of
lemur populations that may eventually turn out to be distinguishable,
although the formal delimitation of
subspecies is an even more hazardous process than recognizing species. Treading warily is strongly
advised.
Groves74 has argued that ‘‘because
the vast majority of infrageneric taxa
are : : : allopatric, the biological species
concept leaves the vast majority of populations inherently unclassifiable; there
is no way to decide whether they are
species or not.’’ This is, of course,
because in allopatry reproductive individuation cannot be demonstrated
(although, as I have suggested, it can be
inferred). Groves thus opts for the diagnosability criterion because it offers
‘‘unambiguous guidelines.’’ But one
then has to ask, ‘‘guidelines to what?’’
The only answer to that is ‘‘diagnosability.’’ To put this in perspective, if
one were to ask what the role of species
is in Nature, it would clearly be inadequate to give the answer ‘‘to be diagnosable.’’ The inescapable reality is that,
in a world in which environments are
in a constant process of flux, allopatry
may be ephemeral, just as are diagnosable variants that have not been individuated by speciation. Employing a logic
not dissimilar to Groves’, Louis et al.,42
in their preamble to describing eleven
new species of Lepilemur on the basis
of genetic distances, explicitly disavow
the use of biological species concepts
because of operational difficulties in
their implementation. Short-circuiting
those difficulties is permissible, they
claim, because their notion of phylogenetic species yields ‘‘evolutionarily significant units.’’ Yet what is the longterm (evolutionary) significance of a
unit that has not been historically
validated—individuated—by speciation?
Where the potential for reticulation
looms, even clearly diagnosable populations can be no more than ephemera, at
best merely potential actors on the evolutionary (as opposed to ecological),
stage.
The conflation of species with diagnosable units is not a problem unique
to Madagascar. The number of primate
species recognized world-wide in some
quarters has more than doubled over
ISSUES
22 Tattersall
the past few decades,74 while actual diversity has, if anything, declined as a
result of human activity. In their discussion of Asian primate diversity, Brandon-Jones and colleagues5 are frank
about the problem in recognizing the
difficulties posed by intraspecific variation: ‘‘In the foreseeable future there is
little likelihood of achieving consensus
on the number of Asian primate genera
and species : : : there is more realistic
hope of reaching agreement on the
number of recognizable subspecies.’’
This pragmatic conclusion was reached
in the service of an ideal of conservation
in which preservation of diversity at all
levels, down to the most local, was the
entirely admirable, if perhaps somewhat unrealistic goal. But from the systematist’s point of view, the problem is
an altogether different one, and in
Madagascar the solution of choice often
seems to have been the promotion of
anything recognizable to species—even
though to do so is to misunderstand the
nature of evolution itself, in which
intraspecific and supraspecific processes are fundamentally dissimilar
and operate according to different sets
of rules. The fact that species boundaries may be fuzzy does not negate the
reality of Nature’s packaging, untidy
though it may be. Spotty sampling may
contribute to the illusion of discreteness; and hewing to a more exigent
notion of species has the added advantage of eliminating the need to explain
why Madagascar should be an islandcontinent bereft of intraspecific primate
diversity.
ACKNOWLEDGMENTS
I thank John Fleagle for prodding
me to produce these thoughts, and for
his astute commentary on an earlier
version. And I am most grateful to Stephen Nash for his elegant illustrations.
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