Systematics of the Lemuridae (Primates, Strepsirhini)

Systematics of the Lemuridae (Primates, Strepsirhini)

Colin P. Groves* Department ofPrehirtov

and

Anthropology, The Australian National Universi~, Canberra ACT 2601, Australia

In the past quarter-century, many studies of Madagascar lemurs have drawn attention to morphological, molecular, karyological, and behavioral similarities between gentle lemurs (genus Hapnlcmur) and ring-tailed lemurs (Lemur catta).The breadth and number of these observations have led us to re-evaluate the affinities of these taxa, and of the family Lemuridar as a whole. After reviewing the literature and examining museum specimens, we identified 32 characters which we consider particularly relevant for understanding the systematics of the Lemuridae. These characters were coded numerically and analwed by various cladistic parsimony procedures. Our findings indicate that, as others ha\re suggested, the genus Lepilemur is probably more closely related to the family Indriidar than it is to anyextant lemurid taxon. For the remaining Irmurids, the evidence favoring a special relationship between gentle and ring-tailed lemurs is striking, but not entirely convincing. A numerical procedure designed to construct confidence intervals on phylogenies, the bootstrap technique, indicates a lack of statistical support for ayy supraspecific grouping oflemurid taxa: the most likely cause for this negative finding is extensive parallel evolution. On the other hand, the analysis of numerous highly parsimonious phylogenies shows that the following supraspecific groups occur in a large majority of them: (1) the two species of Hapalemur: (2) the genus Hapalemur plus Lemur catta; (3) Varecia and the I,. fulvus species-group; (4) Hapalemur plus I.emur plus Vow&; and (5) Lepilemw plus Indriidac. Because of the bootstrap results. we think it premature to alter formally the suprageneric taxonomy of the Lemuridae from presently accepted schemes. However, all ofour analyses reinforce the fact that the Lemur fulrur species-group is highly distinctive by comparison to L. catta. For that reason we suggest the elevation of the_/Suus group to the rank of genus, and we propose the name Petterus for it, with type P. fulous. The incorporation of Petterus in the family Lemuridae, without including any suprageneric groupings, provides a way of indicating the present uncertainty about the phylogenetic afiinities among its members.

Robert H. Eaglen Department ofdnatomy, University ofPuerto Rico Medical School, GPO Box 5067. San Juan, PR 00936. C’.S.A.

Received 20 August 1987 Revision received 15 March 1988 And accepted 17 May 1988 Publication Kegwords:

cladistics,

date September

1988

taxonomy, Lemuridae. parallelism

Journal

ofHuman

Evolution

i 1988)

17. 513-538

introduction In the past most

quarter-century

thoroughly

concentrated forms, these

subjects,

strepsirhines,

extant

on a few major

and the affinities

the subjects

of primate

studied

still unsettled

issue

provides

areas

Olson’s

concerns

the focus

of the

such as the affinities Although

of systematic

has not received

although

topic

issues,

the Strepsirhini

Much

of the Cheirogaleidae.

some other which

systematics,

groups.

interest

sufficient

attention

(1979) work on galagos intrafamilial

for this paper,

in

of early Tertiary there

is the alpha is certainly among

we discuss

been one of the that

period

adapids

is an extensive

have been largely

relationships in which

have

research

to extant

literature

neglected.

taxonomy

an exception. strepsirhines.

the taxonomy

has on

One of of extant Another

The

latter

of the extant

Lemuridae.

Background Most widely Napier

adopted classifications of primates (Simpson, & Napier, 1967; Szalay & Delson, 1979) recognize

* To whom correspondence 0047-2484/88/050513

should

+ 26 $03.00/O

1945; Hill, three

1953; Fiedler,

or four genera

1956;

of extant

be addressed. @ 1988 Academic

Press Limited

514

C.

Lemuridae. valid

Two

taxa.

more recent

argued

assertion

that

polyphyletic. other

its affinities recent

extant

would

and Hapalemur,

Sarich

the

long been

recognized

as

group,

but

genus

Varecia. Of these genera,

the

legitimate

is Lepilemur. Tattersall

questioned

Hapalemur.

Dene

et al. (1976),

& Schwartz

and

Schwartz

&

(e.g.,

1985), have suggested that the nearest relative of is not a lemurid, but the family Indriidae. If true, this

traditional

Lemuridae

& Cronin

(1976)

indriids,

again

and

have

Lemur as a third

the genus

lie with

studies strepsirhines

make

lemurids

treat

have been most strongly

in more

Lepilemur among

studies

have split off L. variegatus as a fourth

affinities

Tattersall

AND R. H. EAGLEN

Lepilemur

genera,

systematic

works

one whose (1974)

of these

Older

P. GROVES

at least

paraphyletic,

that Lepilemur

suggested undermining

the

and

was the sister

monophyly

of

possibly

group

the

of all

traditional

Lemuridae. The balance Lemuridae,

of opinion,

leaving

Lemur and

group

arrangement

tails

canines; elongated and

generally L.

excluded

muzzle;

cling

carried

entoglenoid

greatly

mechanism. this group,

reduced

to

This

however,

the

literature)

has

morphological

and

on

closely

related

school

(1985)

of the

on primate

features

or

a combined

that L. catta shows This

theme

structures

Pariente Mahe

(1975)

on

system,

(1976)

and

(1964)

(1970)

of the reproductive

appears

of the upper

& Buettner-Janusch

hemoglobin,

Rumpler

from the

to a canine

on

Rumpler

and

retinal

Tattersall

a variety

to Hapalemur than

karyotypes

than to other

reinforced

to any other is the finding

members

their earlier lemurid.

ofthe assertion

A remarkable

that a particular

mode

of

& Dutrillaux

(1978) on metachromatic pathways, and Dene systematics. All of these studies note features

(1986) have recently to Hapalemur

two features

of dental

Lemur,

genus

to Hapalemur.

sequences,

and

honing.

resemblances

eruption

first;

isolated

a number

who

well developed

related

in the literature

on

upper

features:

than

only

distinctly

suggestions

characters,

more similar

discerned

listed

and

following

larger

of attributes

long

et al. (1977),

are relatively

to canine

(1972) on morphology premolar

behavioral

& Dutrillaux

a complex

the

molars

process

Hill (1953)

air sinuses,

noted

(1980)

Buettner-Janusch

(1974)

(1978) on karyology, von Hagen Goodman (1978) on immunodiffusion L. catta appears

Eaglen

vague.

Petter

( 1965) on scent-marking

Petter

on vocalizations,

genus, second

monophyly

striking

( 1960) and

Andriamiandra (1974)

Dutrillaux

such a

size; long snouts;

premolars.

a postglenoid

repeated

to large

neonates

and

the

to be rather

incisors;

can be related

from

Hewett-Emmett

& Schwartz

is more

Lemur of the older

in which

& Tattersall

challenge

(1964)

morphology,

Rumpler

Within

opinion;

paranasal

upper

pelage.

sense:

odd and occasionally

&

groups

of which

arises

premaxillae,

upper

social

Schwartz

group,

Andrew

which

from the family

to Hapalemur.

in turn

recent

tended

in the

of the squamosal,

in the work of Bolwig Barnicot

large

to the mother’s

most

principal

Lemur-Varecia

limb,

of

medium

on the posterior

in the broad

process

uniting

Lemur have

membership

large

birth

honing

erect;

from

fairly

from

sometimes

linked

is, the genus

as diagnostic:

a metacone

to the genus

The

taxon

consensus

(that

of the genus

variegatus

arboreal,

unique

a

clade

characteristics

and lacking

largely

represents

definitions

the following

bushy

be removed

questioned.

Taxonomic cited

a monophyletic

of the Lemur-Varecia

been

that Lepilemur should

suggests

Lemur, Varecia, and Hapalemur as its members.

Varecia form

undoubtedly

monophyly indeed

then,

the genera

& in

genus Lemur. that L. catta result

of the

ofkaryotypic

change appears to dominate within many of the major groups of primates. In the Strepsirhini that mechanism of change is Robertsonian translocation. Their model of karyotypic change among Lemuridae unites the L. fulvus species-group, L. catta, and

LEMURID

SYSTEMATICS

515

Hapalemur by a non-Robertsonian translocation not seen in Varecia or Lepilemur. The species of the Lemur @us-group share a single Robertsonian translocation, while L. catta and Hapalemur are linked by a Robertsonian translocation associated with a pericentric inversion. Rumpler & Dutrillaux also note that within the latter group Robertsonian events no longer predominate, and pericentric inversions are at least as common (see their figure 10, p. 93). There is, then, a substantial body of evidence challenging the notion that the genus Lemur is, as a whole, the sister group of the genus Hapalemur. At the very least, the evidence indicates that if the distinctive features of L. variegatus warrant its elevation to generic status, then the equally distinctive features of L. catta and the L.&lvus-complex should also be recognized by corresponding elevation of their ranks. Maier (1980) and Schwartz & Tattersall ( 1985) have echoed this sentiment, although neither of those studies proposed a new nomenclature to reflect this situation. Groves (1974) and Eaglen (1980) suggested the use of the category of subgenus to describe relationships within the genus Lemur.

Materials and methods Both of us subscribe to the systematic philosophy of phylogenetics, which requires that classification reflect, to the greatest extent possible, the best estimates of phylogenetic relationships within a group. After extracting from the literature characters claimed to vary among the taxa examined here, we separately examined skulls and teeth of specimens in the American Museum ofNatural History (RHE), the Smithsonian Institution (RHE), and the British Museum (Natural History) (CPG). The examination of specimens served to verify, and in some cases to permit quantification of, distinctions made in the literature; we also searched for other appropriate characters by this means. We did not attempt to verify soft-tissue features; where our own experience or that of colleagues leads us to be suspicious of such attributes, it is so noted in the text. In the final analysis, we examined 32 characters for the following nine taxa: Lemur cutta (Lc); members ofthe L.&lvus-complex, including L. coronatus, L. fulvus, L. macaco, L. mongoz, and L. rubriventer (collectively Lf); Varecia variegata (Vv); Hapalemur griseus (Hg); H. simus (Hs); Lepilemur spp. (LP); Indriidae (IN); Cheirogaleidae (CH); and Daubentonia (DA). We excluded taxa known only from subfossil material for lack of data on their soft tissues; in a few cases, however, consideration of the subfossils proved helpful in assessing polarity. The characters selected were those which, in our opinion, are most appropriate for evaluating the systematic relationships within the traditional family Lemuridae. While these characters may also indicate something about the systematic affinities of other strepsirhines, they are not balanced by the defining features of such taxa and should not be of Daubentonia to other interpreted as conclusive evidence for, say, the relationship Madagascar lemurs. Character transformation sequences (that is, character polarities) were hypothesized only when we felt that the evidence from outgroup comparisons, or in a few cases ontogenetic evidence, was sufficiently compelling to warrant such judgments. The primary outgroups we considered in interpreting character evolution among the Lemuridae were cheirogaleids and adapids (especially the Notharctinae). Indeterminate character states were coded as such. Detailed descriptions and character codings can be found in the next section. Phylogenetic analyses of these characters were conducted using version 2.4 of David Swofford’s PAUP program (Swofford, 1985). Because the number of taxa analyzed here is

C. P.

516

small

(i.e.,

trees,

and so extract

less than

phylogeny

in this

possibility

1980;

group;

that

necessarily

the

believe

such

that

a subset

by parallel

PAUP

program

(where

tree length were

as short

a consensus

and serves validity

2.7 of the BOOTM in the program

In

to

addition

The

character then

the

rooted

obtained

states with

interval.

this

(five times

we

a technique a set

sets

entirely.

groups

using

in this manner,

is taken

occurred

to be statistically of characters the greater

was implemented package,

most

trees obtained

the characters,

the minimum

n

matrix

For each of these

that

the number

of n

containing

is obtained

obtained

PHYLIP

for a trees

set of trees,

from the original

of that group

in Felsenstein’s

change

in 95% or more ofthe larger

the

of numerous

is, r data

between

to are

in this study,

of the phylogeny

The

appears

is little reason

procedure,

the r phylogenies

the correlation

of almost

is to employ

characters

will be. This procedure

and the

by employing with

number

the original of replicates

documentation). explicitly

(Sneath

available

that

occurs

range

in any of the trees.

bootstrap

the monophyletic

100 times

characters

coefficient

of NTSYS-PC, was

some

of its members

From

will be omitted

From

If a group

program

resampled

suggested

matching

is not by

of taxa

of evolutionary

occurring

the

an estimate

as a confidence

of the procedure

set of 32 characters

phenetically.

rral

than a given tree length

of parallelism

In

and others

there

the content tree.

groups

for the monophyly

and the lower

trees,

to analyze

set, some

containing

a broad

of taxa analyzed

replacement;

procedures.

the evidence

of replicates,

analysis

times,

is developed

from the replicates,

version

phylogeny

subset

to or shorter

parsimonious

such data

in the set of r phylogenies.

statistical

is

is a very

problem

the relationships

number

1985).

(or replicates),

parsimony

tree

or that

the problem with

For every

is to examine

parsimonious

able

as the most

r times

of data

Wagner

significant,

evolution

there this

of the total amount

we were

one or more

sets

frequently

ofstrepsirhinc

parallel

of character

circumvent

trees equal

estimate

(Felsenstein,

are created.

standard

ofall

way of circumventing bootstrap

will be duplicated

most

of all monophyletic

is resampled

resampled

that

is, if a particular

For the small

the recovery

Consequently,

almost

as the

characters

of all possible

studies

of parallelism,

to

That

by chance,

is a numerical

An alternative

number

occurs

the frequencies

characters

parsimony

Previous

indicated

level

of parallelism

of nearly

evolution.

permits

set of characters).

known

have

high

possible

phylogenies.

in a wide spectrum

which

the relative

interpretation

is

the problem

consistently

determined

EAGL.EN

subterfuges. parsimonious

obscured

1983)

of this it

H.

phylogenies.

parsimonious

One way to ameliorate maximally

Tattersall,

However,

R.

to evaluate

parsimonious

because

most

correct.

methodological

AND

12), it is possible the most

(Eaglen,

rampant

GROVES

phylogenetic

were

& Sokal,

from

A phylogenetic

a hypothetical

primitive

this hypothetical

we

also

analyzed

the

data

to a UPGMA analysis based on a simple with version 1 .O1 1973); th e analysis was performed

F. J. Rohlf.

by including

we consider

analyses,

subjected

ancestral

for the Lemuridae;

ancestral

interpretation taxon

of the phenetic

consisting

the resulting

of all the

phenogram

was

taxon.

Character descriptions Below are the characters finally adopted used for each feature follows its description; preceding character

section. polarity,

for phylogenetic analysis. The coding scheme taxon abbreviations are those described in the

Where we feel reasonably confident about the presumed primitive character state has

our been

interpretation marked with

of an

LEMURID

asterisk.

Taxa

character

in which

coding

questionable

the

scheme;

distribution

taxa

are tagged

with

of a feature

in which

a question

incisors. This character

interpretation

rests largely

no data

were obtained

for adapid

2 Absent: (2)

small:

small:

distal

character among

*0 No hone:

CH,

This

character

wear

to the upper

canine with

and

crown

adapids,

Ps, most

Pronycticebus and

the anterior premolar

honing to treat

living

1 Molariform:

not

verify

related

in which

indriids

three

is nearly

Thus,

of this tooth

latter

measured

equal

or slightly with

from its from

the

of the corresponding

reduction

& Delson,

both outgroup

1979); larger

of P* relative more

to

commonly,

than

Ps. A reduced

the development

of a canine

and functional

considerations

lead us

condition.

the posterior

premolars

upper

also occur

strepsirhines;

and lower premolars among

we consider

Tattersall

the permanent

galagids,

were molariform

but are otherwise

this condition

rare

derived.

DA

these

teeth develop;

The

eruption

permanent

& Schwartz

premolars sequence

premolars;

& Schwartz,

1974).

erupt,

we excluded

(1974),

eschewing the latter

for indriids

however, We follow

feature species

the sequence

those

authors

differences

differences

because

is suspect,

subfossil

exhibit

we coded reported

since

no extant

presumably indicated

in treating

in

we could closely for extant the 2%4-3

as primitive.

*0 Sequence

2-4-3:

Lf, Vv. CH

1 Sequence

4-3-2:

Hg, Lc, LP, IN?

(6) Molar hypocones (Figure 2). We discriminated total

as

This

does not occur

surface

substantial

correlated

(i.e., Archeolemur, Hadropithecus)

(Tattersall

sequence

complex

as a percentage

(Szalay

Lc, Ll; Vv, LP, IN, CH,

it ourselves.

to indriids

as well

premolar.

Hg, Hs

in which

possess

The

(the

demonstrate

partly

(5) Premolar eruption sequence. Following

indriids

feature.

diameters

Muhgarita

premolar

whether

posterior

*0 Not molariform:

the sequence

lower anterior

Hg, Hs, Lc, LP, CH

and extinct

in the sequence

of correlated

premolar,

Lf, vv

(4) P4 shape. We noted or not. Molariform

a complex

anterior

for strepsirhines.

this area

of P’ as a derived

*0 84 to 103%: 1 50 to 66%:

lower

the area of the buccal height

be at least

(see below).

the reduction

among

since

DA

a few genera

upper may

mechanism

represents

the

the previous

and expressed

area of Ps. Among however,

in cheirogaleids,

Lc, Lf, Vv

junction),

notably

on

and to the caniniform

Hg, Hs, LP, IN, CH,

present:

cemento-enamel

likely

facet

and is very likely derived

mesiodistal

anterior

of a size extreme

IN, DA

(3) P2 reduction (Figure 1). W e computed maximum

( 1986). The

is taken from the data of Eaglen

on the absence

a distinct

adapids,

1 Hone

is

material.

may also be correlated known

in the

LP

including

diastemata

omitted

of the feature

Lc, Lf, Vv, Hg

Canine honing mechanism.

features,

are

or homology

mark.

( 1) Relative size ofupper

1 Significantly

is unknown

the distribution

polarity

*0 Not significantly

517

SYSTEMATICS

absence

from all upper

molars,

presence

three of large

possible

conditions

and well-formed

for this feature: hypocones,

or the

518

C. P, GROVES AND R. H. EAGLEN

Figure 1. Crania of Lemur in lateral view. Above: Lemurcatta (NMV R-2955-6). Below: Lemur filcus (NMV 2605). Scale represents 50 mm.

LEMURID

SYSTEMATICS

Figure 2. Crania of Lemur in inferior view. Lemur catta above, Lemurjihus Figure 1. Scale represents 50 mm.

519

below: same specimens

as in

520

C. F.

GROVES

AND

R.

H.

EAGIXN

occurrence of small elevations on the distolingual cingulum. The hypocone if present is invariably seen on Ml, and variably on Mg. The presence of a hypocone on the upper molars is characteristic of many early Tertiary primates, including a variety of adapids and plesiadapoids (Szalay & Delson, 1979). The occurrence of small, apparently cingulum-derived hypocones in the early notharctine Pelycodus (Szalay & Delson, 1979) and in cheirogaleids leads us to treat this condition as primitive for strepsirhines. 0 Absent: Hg, Vv, LP *l Small: Hs, Lc, Lf, CH 2 Large: IN, DA (7) Molar pericones. Presence of this cuspal elevation on the mesiolingual aspect of the cingulum was coded similarly to the previous character. The morphology of Vurecia is somewhat problematic; its molars show a complete cingulum on the lingual aspect, but the cingulum is subject to wear which obscures the presence of cuspules. Occasionally one can find young specimens in which the cingulum is cleft just lingual to the apex of the protocone, suggesting the presence of a small pericone. The pericone is rare among early Tertiary primates and extant strepsirhines, and we therefore consider its presence in any form to be a derived condition for the Strepsirhini. *0 Absent: Hg, LP, IN, CH, DA 1 Small: Hs, Lc, Vv? 2 Large: Lf (8) M3 reduction. We measured maximum mesiodistal and buccolingual diameters of M* and Ms, and computed cross-sectional area of the latter as a percentage ofthe former. Most adapids show a modest degree of reduction of the posterior upper molar, which we take to be the primitive condition. *0 73 to 80%: Hg, Hs, Lc, LP, CH, DA 1 49 to 63%: Lf 2 30 to 50%: Vv, IN (9) Molar talonid basins. Following Schwartz & Tattersall (1985), we noted situated crests tend to seal off the talonid basin on that side. *0 Basin open lingually: Hg, Hs, Lc, CH, IN 1 Open distally or not at all: Lf, Vv, LP

if lingually

(lo) Zygomaticofucial (mulur) foramen. We measured the greatest diameter of this foramen on one side (usually the left). Occasionally, a specimen will exhibit two (rarely, three) small foramina instead of a single large one; in such cases, the diameters of the multiple foramina were summed. One of us (RHE) dissected specimens of Lemur cutta, L.&lvus, and H. griseus to find the basis for the differences in the size of this foramen; in every case, the opening was filled mainly with fatty tissue. The zygomaticofacial branch of the zygomatic nerve passes through the opening, either as a single trunk or already split into rami; the nerve is, however, quite small relative to the size of the foramen. Specimens of L. cotta and H. griseus, but not L. jihus, also transmit a minute branch of the transverse facial artery; again, the extremely small caliber of this vessel indicates little correlation with the size of the surrounding foramen. We also considered if, in taxa with a large opening, the region might be under net tension and therefore subject to resulting bone loss (Oxnard, 1971). Some tension is likely to be involved, since the origin of the masseter is traceable to a point immediately inferior to the

LEMURID

foramen.

Close inspection

Museum

of Victoria

thicker

bone

orbital

marginal

shifted

than

dificult,

and The

leaving

we have

foramen our

coding

foramen

orbital

plate-like

seems

to be the

margin

is slightly

cheekbone

in the

or absent

from the

to run through

in this region

to differences

is small

absent:

absolute

in adapids

proper.

would

be very

size

of the

(Gregory,

1920:

DA, IN Lf, LP

1.8 to 3.2 mm:

Hg, Hs, Lc, V\r

of paroccipital

paroccipital among

*0 Small:

living

of presphenoid

they may diverge

suface

other

the least

the greatest to code;

of the cranial

diverge

1 Sutures

nearly

2 Sutures

converge

just

strepsirhines).

shape

pterygoid, rostrally: parallel:

latter

elongate,

paroccipital a derived

of the presphenoid

taxa which

exhibit

H. griseus exhibits

admitting

that

the

rather

or

broadens

the former

condition,

more;

Lemur cattu

more caudally

than in the

somewhat

of the sutures. directions

much

may approach

(as in Lc, Hg, and Vv),

surface

but this occurs

among pterygoid

Such relationships of the sutures

of the subtlety

may

are

between be lost in

Lf, LP, IN, CH

rostrally:

is not

pterygoids

to the vomer

for the profile

differences and medial

Hg strepsirhines,

the posterior

apparent

the posterior

bulla terminates

in Early

Tertiary

margin

in a tapered primates,

and

of the bulla

is

bony spicule. we therefore

it derived.

*0 Blunt:

1 Tapered:

I-f, Vv, LP, IN Hs, Hg, Lc, CH

(14) Interorbital projile. In most strepsirhines concave interorbital surface, contrasting with inflated,

an

Lc, Vv

while in others

morphology

The medial

caudal

to note the different

(13) Shape of the auditory bulla. In some and rounded,

base.

Among

while

of constriction,

a goblet-like medial

are conspicuous basisphenoid,

so that the visible

constriction,

degree

There

of the presphenoid,

in the end we opted

and

so. *0 Sutures

consider

of either A blade-like

and is thus likely to represent

to medial ptevgoid.

from the midline,

taxa, effecting

presphenoid

presence

projection.

DA

the presphcnoid

(as in Lfand

Vurecia shows

difficult

and fossil primates,

in the arrangement

constricting

evinces

the

Hs, Hg, IN

on the external

rostrally

noted

flange-like

strepsirhines.

(12) Relationship

midline,

We

or a small

Lc, Lf, Vv, LP, CH,

1 Large:

strepsirhines

process.

process,

is rare among

bones

CH,

2 Diameter

condition

lack

the

differences

0.2 to 1.2 mm:

process

The

pierce

1 Diameter

Development

(11)

blunt

to

functional

appears

In L. jiulvus this bone

back; in L. cattu the lateral

underlying restricted

group

1958).

blade-like

doing

the

of the L.&lvus-complex

in the latter

of the former.

is shifted

zygomaticofacial

*0 Foramen

other

opening

which

of possible

foramen. Gazin,

that the tiny foramen

the large

forward,

Quantification

521

of skulls of L. catta and members

shows

bone,

SYSTEMATICS

creating

such

Strepsirhini.

a bubble-like

a dilatation,

and

dilatation we

believe

the orbital rims rise above a somewhat others in which the interorbital region is

of the middle this

third of the skull roof. Notharctines

represents

the

primitive

condition

for

522

C. P. GROVES

*0 Orbital 1 Orbital

AND

R. H. EAGLEK

rims intergrade with frontals: Lc, Hg, Hs, Vv, LP, CH, DA rims rise above frontals: Lf, IN?

(15) Relative facial length. The length of the facial skeleton is the most conspicuous difference between the genus Lemur as conventionally defined (especially ifmade to include I’urecia) and other putative lemurids. We quantified this feature by measuring from prosthion to the anterior margin of the orbit, and computing the ratio of that measure to total skull length, measured from prosthion to opisthocranion. Many subfossil lemurids data to substantiate this exhibit apparently long faces, but we lack the quantitative impression. The varied distribution of character states for this feature and the lack of sulhcient data from outgroups precludes a convincing decision about the polarity of this feature. 0 Very long face, over 54%: Lc 1 Long face, 50 to 54%: Lf, Vv 2 Short face, 45 to 50%: Hg, LP, IN, CH 3 Very short face, under 45%: Hs, DA (16) Pigmentation of ocular jkndus. This character and the next are based on the work of Pariente ( 1970). Using his scheme, we coded the fundus of the eye as either unpigmented, spotty, or strongly pigmented; however, we question whether the “spotty” state is truly intermediate. We suspect the lack of pigmentation to be correlated with nocturnality, and thus more likely to represent the primitive condition for strepsirhines. *0 Unpigmented: IN, CH, DA 1 Spotty: Lc, Hg 2 Strongly pigmented: Lf, Vv (17) Ocularfovea. We coded the presence or absence of a well-defined area centralis in the retina, leaving open the question of whether this area is homologous to the haplorhine fovea. The rarity of this structure, which presumably enhances diurnal visual acuity, leads us to treat it as a derived condition among the Strepsirhini. *0 Absent: Lf, Vv, LP, IN, CH, DA 1 Present: Hg, Lc (18) OS centrule. In most strepsirhines, the OS centrale is a distinct bony element, but in some taxa it is fused with the scaphoid. The distribution of this feature among early Nevertheless, Matthew (1909) noted that a “free” OS Tertiary primates is unknown. and suggested that this conditions was centrale was present in primitive creodonts, primitive for placental mammals. The tree shrew Tupaia has a “free” OS centrale uouffroy & Lessertisseur, 1959). These observations, in conjunction with the rarity of fusion within the Strepsirhini, lead us to treat fusion of the OS centrale with the scaphoid as a derived character state. *0 Separate: Lc, Lf, Hg, Hs, Vv, CH, DA 1 Fused: LP, IN (19) Baculum.

of most strepsirhines is a simple rod-like structure. In H. and separate prominences. In some strepsirhines, the baculum diverges into two distinct crura, which in cheirogaleids recurve toward the midline to form a bacular foramen. A simple rod-like baculum is almost universal among mammals and is most likely primitive for strepsirhines. The baculum

griseus, the distal end shows two rounded

LEMURID

*0 Simple:

(20)

523

SYSTEMATICS

Lc, Lf, Vv, DA

1 Incipiently

bilid:

2 Divergent:

LP, IN, CH

Hg

Penile spines. Following

the description

of Hill ( 1953), we noted

the presence,

size, and

number of spiny projections on the body of the penis. Penile spines are sporadically present within Primates and many other mammalian groups, and their presence is most likely primitive for the Strepsirhini. *0 Spines

(21)

numerous:

few, small:

2 Spines

absent:

elements

Lc, CH,

DA

Lf, LP, IN

Hg, Vv

Scrotal skin. We coded

glandular

(22)

large,

1 Spines

the presence

or absence

0 Kaked,

wholly

1 Furred,

glandular

2 Furred,

not distinctly

glandular:

(23)

Neck glands.

We

in primates

part

leads

have

that

gland

The

antebrachial papilla

gland

in the female.

among

primates

is a derived

structures;

presence

Rumpler

of these

glands.

&

Their

is derived.

the glandular

system

is associated

with

According

to Petter

an epithelial

makes

glands.

it highly

limbs

or distal

spur

et al. (1977),

but homologous

mammals

of the upper in the middle

in the

Hupulemur

Distributional

likely that presence

of

DA

Hg, Hs, Lc

placental

vibrissae

1918), the vast majority to interpret

CH

these

mammals

structures are thought

as present,

genal,

of primates

lack the interramal

the polarity

Vv, DA

superciliary,

of this feature

absent,

or rudimentary.

to have had a full complement

(mystacial,

Hg, Lc, Lf, LP, IN

1 Rudimentary: 2 Present:

at the base of the

condition.

Lf, Vv, LP, IN, CH,

primitive

0 Absent:

of such

the homology

smaller

and other

Interrumul vibrissue. We coded

are reluctant evolution.

opens distally.

part of the arm, and another

H. griseus in possessing

from

I Present:

sets of tactile

their

fully developed,

in the proximal

and with a smaller

Although

urethra

and opens

or absence

questioned

DA

of the forearm.

*0 Absent:

(25)

presence

us to suspect

ofa scent

glands

the female

the clitoris

Hs, Vv, 11L

considerations these

the

however,

Upper limb glands. When

simus differs

of

Hg, Hg, Lf, Vv, CH

Lc, Lf, Hg, LP, CH,

1 Present:

male,

noted

(1971),

*0 Absent:

(24)

the presence

Hg, Lc, Vv

Andriamiandra

consists

and

LP, IN

glandular:

Female urethral path. In some strepsirhines,

rarity

hair,

Lc, DA

at base:

clitoris, while in others it tunnels through 0 At base: Lf, LP, IN, CH, DA

1 Distally:

of scrotal

in the skin of the scrotum.

interramal,

and

and carpal

groups.

or the next

in terms

of five

carpal-Pocock, Therefore, of strepsirhine

we

C.

524 Carpal vibrissae. Coded

(26)

GROVES

as present

0 Absent:

LP, IN, DA

1 Present:

Hg, Lc, Lf, Vv, CH

Throat sac. We

(27)

homology

coded

for the

presence

Hg, Hs, Lc, Lf, LP, DA

1 Present:

Vv, IN, CH

Lung lobes. Strepsirhines below.

exhibit

left, 3 right:

Hg

2 3f

left, 2 right:

IN, DA

of a “tubuliform

comm.

to RHE)

among

strepsirhines,

has

indicated

structure,

although

the

that

1 Present:

Hg, Lc

Electrophoresis

two fractions hemoglobins

of some

lorisiforms

Znfant carriage. teeth,

it is subject 1 Oral

There birth,

Paranasal

species-complex

the distribution

may well be much

taxa in which

those in which

also separated

are

several

strepsirhine as the infant

Vv, LP, CH,

as

partitioning

of

of this

more

feature

widespread.

hemoglobin

separated

into

it did not (Buettner-Janusch

1974).

It should

into distinct

be noted

&

that

the

fractions.

ways

in which

neonates

are either

fur. We have coded progresses

this

feature

kept

the neonatal

in its locomotor

could

in nests,

be

carried

pattern,

treated. by the although

development.

DA

Hg

Lc, Lf, IN sinuses. Alone exhibit

among

varying

strepsirhine

degrees

palatine and presphenoidal sinuses the facial skeleton of L. jidvus

of inflation

of the paranasal

sinuses:

lie well inferior

to the midpoint

of the orbital

maxilla. To minimize This unusual feature, out relationships

primates,

members

of paranasal

of the Lemur fulvus

air sinuses,

especially

(Hill, 1953; Maht, 1976). Other distinctive and its allies may be correlated with

pneumatization

of that group. *0 Sinuses 1 Sinuses

about

& Hewett-Emmett,

or cling to the mother’s

carriage:

2 Cling:

of the lungs,

Lf, Vv, IN, CH

to changes

0 Nested:

those

versus

1964; Barnicot

after

incomplete

DA

electrophoresis,

*0 One component: 1 Two: Lc, Hg

Immediately

skepticism such vestiges

of hemoglobin. We noted

during

Buettner-Janusch,

in the lobulation

left lung reflects

system”

strong

suspecting

Lf, Vv, LP, IN, CH,

sorting

of this

Andriamiandra (1972), we coded for the presence at the level of the ovary. Luckett (pers.

reticular

0 Absent:

(32)

or absence

ofthe

Wolffian vestiges in ovary. Following

or absence

mother’s

EAGLEN

Lc, Lf, Vv, CH

1 3f

(31)

H.

one of three patterns

The 3+ characterization

one of the lobes. 0 4 left, 3 right:

(29)

R.

or absent.

0 Absent:

(28)

AND

is very dubious.

indicated

(30)

P.

in the>/vus-group,

the lacrimal

rim, and the nasals

grade

foramen smoothly

the

features of increased comes

to

into the

the effect of such correlations, we have coded only the sinus inflation. which is almost certainly derived and perhaps quite important for within

not inflated: inflated: Lf

the L.&lvus

complex,

is included

Hg, Hs, Lc, Vv, LP, IN, CH,

DA

here as an autapomorphy

LEMURID

Table

1

Data matrix

525

SYSTEMATICS

for characters

discussed

in text’

HHLLVLICD g s c fvPNHA

Character

1?1112000 00 1 000110x0x 110000000 1?100110x 011100212 011210000 0 0 0 000120200 222121000 110000100 2?101000? 1 1 1 000100100 230112223 1?122?000 1 ! 1 000001100 1’0002220 250121100 220221120 1?1010000 0 1 0 1 1 1 0?0010021 1?1110010 0 0 0 1?000?202 1?1000000 1?100?0?? 1?2200200 0 0 0

1 2 3 4 5 6 7 8 9 10 11

Upper incisor size Canine honing mechanism P2 reduction P4shape Premolar eruption sequence Molar hypocones Molar pericones Molar talonid hasins Ms reduction Zygomaticofacial foramen Paroccipital process 12 Presphenoid shape 13 Bullar shape 14 Orbital profile 15 Relative facial length 16 Pigmentation ofocular fundus 17 Ocular fovea 18 OS centrale 19 Baculum shape 20 Penile spines 21 Scrotal skin 22 Female urethral path 23 Neck glands 24 Upper limb glands 25 Interramal vihrissae 26 Carpal vihrissae 27 Throat sac 28 Lung lobes 29 Wolfian vestiges in ovary 30 Hemoglobin electrophoresis 3 1 Infant carriage 32 Inflation ofparanasal sinuses

1

10

0

0

0

1

1

1

0

0

x

0

0

0

0

1

?

0

0

0

0

0

0

0 0

1 0

0 0

1 0

0 0

0 0

0

1

0

1

1

0

1

0

0

0

0

0

1SeeFigure 3 for taxon abbreviations; Derived

The

characters

summarizes other

just

their

characters

Lemuridae,

excluded

which

may have

variable

for that

form

In addition

as an entoconid

the

be quite

basis

some

Schwartz

relevant

for

X = not applicable.

the

ensuing

analyses;

we feel obliged understanding

for various

reasons.

Table

to mention the

1

some

systematics

Metastylids

of

are found

ofHapalemur, Lemur catta, and indriids; they are of the L. &lvus-group, however, and were

species

& Tattersall by suggesting

is in fact

for

characters,

included

of both species

distribution

? = unknown; in bold type.

to those

not been

among

reason.

of metastylid

identified

described

lower molars

intraspecifically

states indicated

coding.

but which

on the anterior

question

character

homologous

(1985) that

have

further

complicated

in Lepilemur, the structure

with

the metastylid

seen

the usually

in indriids,

Hapalemur, and Lemur catta. Tattersall & Schwartz (1974) noted that Hapalemur griseus resembled L. catta, but not Lepilemur, in the sequence in which the permanent premolars develop;

we bypassed

this feature

because

of its likely

high

premolar eruption sequences. One of us (RHE) has heard engage in the curious behavioral pattern known as “stink also occurs

among

wild and captive

Lemur catta; the rumor

correlation

with

permanent

reports that captive H. griseus fighting” (Jolly, 1966), which has not been verified,

however.

526

C.

P.

GROVES

AND

Quantitative

R.

H.

EAGLEN

analyses

as coded in Table 1, by performing a We began our analysis of the characters, branch-and-bound search for the shortest possible tree with Swofford’s PAUP program. The analysis yielded live maximally parsimonious trees, with a length of 85 steps and a consistency index of 0.553; Figure 3 shows these trees. The consistency index is rather low and implies that nearly half of the evolution of these features required parallelism or reversal. Extensive homoplasy for strepsirhine phylogeny is not surprising (Eaglen, 1980, 1983; Tattersall, 1983). Although the level of homoplasy suggested by the consistency index is quite high, it is noteworthy that the same cladistic relationships occur among lemurids (not including Lepilemur) in all five trees. We next employed the bootstrap procedure to see if there is significant evidence for the monophyly of any of the taxa shown in Figure 3. The consensus tree obtained from a bootstrap analysis with 100 resamplings of the data set is shown in Figure 4; the affinities of Daubentonia and the Cheirogaleidae were indeterminate in that analysis, and hence those taxa are not shown. More importantly, the bootstrap analysis indicates that none of the taxa shown in Figure 3 are sustainable as monophyletic groups at a 95% level of significance. Because the bootstrap involves character resampling, we decided to perform the procedure again, on the off chance that our first effort may have reflected a particularly odd set of resamplings. Four additional runs of the bootstrap provided comparable results-no statistically significant evidence for monophyly for any group of strepsirhines (beyond the obvious monophyletic groups implicit in the study, such as the family Indriidae). The nearest approach to a 95% confidence interval occurred in one run where the two species of Hapalemur were linked in 89% of the resamplings of the data. The results of the bootstrap provide cold comfort, and are no doubt explained by the extensive homoplasy in our data. Because of the homoplasy it is reasonable to suspect that the most parsimonious phylogeny, or set of phylogenies in this case, may not represent the true tree. Thus, we searched for trees that were almost but not quite the shortest, and calculated the frequency of all monophyletic subgroups for this larger set of nearly most parsimonious trees. The five shortest trees were 85 steps in length; we found seven additional trees with a length of 86 steps, 37 trees of 87 steps, and 69 trees of 88 steps. We then tabulated the frequency of all groups occurring in each of those trees. A few trees contained a zero-length branch, implying a trifurcation at that point; in such cases each of the three alternative pairings of the taxa involved in the trifurcation was tabulated. The results are summarized in Table 2. Among the 118 nearly shortest trees we examined, a “lemurine” clade linking the various species of Hapalemur, Lemur, and Varecia occurred in nearly 80%; more impressively, this clade occurred in nearly all of the 49 trees whose lengths ranged from 85 to 87 steps. What does this mean? The bootstrap tells us that we cannot have confidence in a statistical sense that a lemurine clade is valid, presumably because our data show extensive homoplasy. That homoplasy by itself makes us suspicious of inferences based on one or more m,aximally parsimonious trees alone, since a change in the interpretation of a single character can cause a different tree to become the most parsimonious (Eaglen, 1983). However, even if one or a few characters were interpreted in a different way, the most parsimonious trees would still be no more than a few steps longer than the tree obtained in

LEMURID

Hg

Hs

3A

CH

3A

CH

Lc

DA

Lf

527

SYSTEMATICS

vv

3A

LP

PA

LP

3A

CH

DA

CH

DA

LP

DA

LP

CH

LP

E

Figure 3. The shortest cladograms (3E3E) for the data of Table 1. The relationships among lemurine taxa shown in 3A are identical in the live cladograms from 3B to 3E. Abbreviations: Hg, Hapnlemur grism; Hs, H. simus; Lc, Lrmur catta; Lf, L.fuluus-complex; Vv, Varecia uariegnta; 3A, the “lemurines” as shown in Figure 3A; CH, Cheirogaleidae; IN, Indriidae; LP, Lepihur spp.; DA, Daubntonia.

LP

Figure 4. Bootstrap phylogeny for the data of Table 1. Numbers at interior nodes reflect percentage of replicates in which group occurred, averaged over live runs of the bootstrap procedure; thus, for example, in 83% of the resamplings of the data performed by the bootstrap, the two species ofHaPalemur were linked to each other in the shortest tree. Abbreviations as in Figure 3; the affinities of Daubentonia and the Cheirogaleidae proved indeterminate and are not shown.

the original

analysis;

the shortest

tree(s),

and when

we examine

we find a lemurine

clade

all the trees to occur

that are nearly in a great

majority

equal

in length

to

Thus, that the among a

of them.

even though we cannot say with any plausible degree of statistical certainty lemurine clade is monophyletic, we can say that a lemurine clade predominates broad range of phylogenies which minimize “excess” evolutionary events. Thus, using the kind of logic outlined above, we can point out that within this lemurine clade, there is remarkable consistency in the relationships of taxa to each other. The two species of Hupalemur form a sister group in nearly 85% of the 118 very short trees we studied. An even larger percentage of those trees link the Hapalemur species to Lemur catta. Finally, the species of the L.>lvus-complex are allied with Vurecia in over 75% of the trees we analyzed. It is worth noting that these taxa occur in the consensus tree obtained by the bootstrap procedure as well. In addition to the lemurine relationships noted so far, our findings also indicate a possible close affinity between Lepilemur and the Indriidae. That grouping occurs in over 70% of the 49 trees between 85 and 87 steps, but drops to a little more than 50% when trees a step longer are included. Although our findings suggest the existence of this clade, they provide little evidence to indicate its affinities. The most likely candidate arising from our analysis is Daubentonia, but we must caution that we selected characters which vary systematically among the Lemuridae. Thus, characters which have an important bearing on the affinities of non-lemurid taxa were not included here if they do not vary among the Lemuridae, and our findings concerning nonlemurids should not be taken too seriously. There is one aspect of negative information conveyed by our analysis which should be

LEMURID

Hg

529

SYSTEMATIC3

HS

Figure 5. Rooted phenogram

underscored.

For

j&us-complex

grouping

as we coded Lemur as many for the

for doing

immunodiffusion

1976). We analyzed

authorities

& Sokal

(1973),

containing

character

states

this study

(Figure

have emphasized

5) shows

including

of our

data,

the Unweighted

for rooting

the same

envision

Lemur

L.

the

no support

for

it. Furthermore, Varecia);

(including

primitive

purposes

albeit in similar

Pair-Group

that

a phylogenetic corroborating

fashion

(or et al.,

(Dene

Method

a hypothetical

for the Strepsirhini.

relationships

with

ofpotentially

has been analyzed

we consider

we found

we analyzed.

analysis

using

of Lemur catta and

currently

genus

DA

as in Figure 3

at. Thus,

so was that one source

study,

our characters

of Sneath

1. Abbreviations

a grouping

traditional

a phenetic

Our reason data,

them,

up in only 2% of the trees

we performed

interpretation.

for the data of Table

in any of the trees we looked

no support

showed

falsifying)

data

of the genus

almost

Finally,

the

did not occur

the monophyly we found

CH

LP

(UPGMA)

ancestral

taxon

The tree obtained

for the various

lemurid

taxa

that

for we

so far.

Systematics Phylagenetic relationships Our

analyses

Hapalemur, strepsirhines, This

suggest

the

Lemuridae,

as a phylogenetic

grouping

of the

genera

Lemur, Varecia, and Lepilemur, is not strictly monophyletic. Among extant the affinities of Lepilemur, appear closer to indriids than to other “lemurids”.

is not a novel

serological

that

data.

finding. Schwartz

morphology,

concluded

Megaladapis,

and these

that taxa

Dene

et al. (1976)

& Tattersall

came

(1985),

the most likely sister in turn

form

the sister

to the same conclusion on the basis of in their study of strepsirhine dental group group

of Lepilemur is the subfossil of the Indriidae.

genus

C. P.

530 Table 2

Percentage of monophyletic

GROVES

AND

R. H. EAGLEN

subgroups found among the 118 shortest trees. Tree length

Grouping

85 (n = 5)

<86 (n = 12)

S87 (n = 49)

<88(n= 118)

Hg Hs LfVv IN LP DA IN Hs Lc Hg Lc CH DA CHIN DA LP

100.0 100.0 100~0 0.0 0.0 0.0 0.0 0.0 0.0

100.0 58.3 83.3 8.3 0.0 0.0 0.0 0.0 0.0

83.7 73-5 71.4 10.2 20.4 16.3 2.0 0.0 2.0

84.3 76.5 54.9 20.6 15.7 13.7 5.9 3.9 2.9

Hg Hs Lc DA IN LP LP LfVv CH DA IN CH IN LP HS LfVv Lc Lf vv CH Lf Vv

100.0 80.0 0.0 0.0 0.0 0.0 0.0 0.0

100.0 75.0 0.0 0.0 0.0 0.0 0.0 0.0

89.8 53.1 2.0 0.0 6.1 0.0 4.1 0.0

89.2 42.2 5.9 4.9 3.9 2.9 2.0 I.0

0.0 20.0 0.0 0.0 0.0 0.0 0.0

41.7 25.0 0.0 0.0 0.0 0.0 0.0

16.3 16.3 10.2 6.1 0.0 0.0 0.0

18.6 12.7 4.9 4.9 4.9 3.9 1.0

100~0 0.0 0.0 0.0

100.0 0.0 0.0 0.0

98.0

0.0 0.0 0.0

78.4 2.9 2.0 1.0

CH Hg Hs Lc Lf Vv LP Hg Hs Lc LfVv DA IN LP Hg Hs Lc IN Hg Hs Lc Lf Vv DA Hg Hs Lc LfVv

60.0 0.0 0.0 0.0 0.0

50.0 8.3 0.0 0.0 0.0

42.9 14.3 0.0 2.0 2.0

29.4 27.5 3.9 2.0 1.0

IN LP Hg Hs Lc LfVv CH LP Hg Hs Lc LfVv CH DA Hg Hs Lc LfVv CH IN Hg Hs Lc Lf Vv CH DA IN LP Hg Hs Lc DA LP Hg Hs Lc LfVv

0.0 0.0 20.0 0.0 0.0 0.0

8.3 0.0 16.7 0.0 0.0 0.0

14.3 6.1 12.2 2.0 0.0 0.0

18.6 11.8 8.8 2.0 2.0 1.0

CH IN LP Hg Hs Lc LfVv DA IN LP Hg Hs Lc LfVv

40.0 20.0

41.7 16.7

42.9

36.3 22.5

Hg CH Hg Hg CH LP IN

Hs Lc Vv DA IN LP Hs Lc Lf Lc Lf Vv Hg Hs Lc Hg Hs Lc LP LfVv

Hg Hs Lc Lf Vv IN LP Hg Hs Lc DA IN LP LfVv CH DA IN LfVv

20.4

We expect some investigators to consider rather more controversial our assertion that the genus Lemur is at least paraphyletic, or perhaps even polyphyletic. Our parsimony analysis indicates that the sister group of L. cattu is the genus Hapalemur. Of course, that relationship has been hinted at in many other studies of strepsirhine morphology, as we indicated early on in this paper. Our conclusion is buttressed in particular by the immunodiffusion study of Dene & Goodman ( 1978), and by the karyological studies of Rumpler & Dutrillaux (1986).

LEMURID

SYSTEMATIC3

531

We can identify only two plausible derived characters uniting the species of the genus (and Varecia as well): a complex of features associated with a canine honing mechanism, and relative elongation of the facial skeleton. The polarity of the latter feature is less than certain. Derived features which unequivocally link L. catta with the L. fulms species-complex are nonexistent, as far as we have been able to tell. Surprisingly to us, many studies which assert the monophyly of Lemur (with Vurecia excluded) simultaneously go to great lengths to enumerate differences between L. catta and the L. j&us-complex. Seligsohn (1977), for example, pointed out numerous differences in molar morphology betweeen these taxa, and ascribed those differences to distinctive mechanical functions and biological roles. Schwartz & Tattersall (1985) o ffer extensive description and analysis of differences in dental morphology between the catta and fuhus groups, but do not include a single derived character uniquely linking the two! Admittedly, there are few derived characters which unequivocally link Hapalemur and L. catta. The most obvious are the scent-marking glands of the arm and forearm, the presence of an ocular fovea, and the electrophoretic behavior of their hemoglobins. The distribution of the latter two features is unknown in H. sinus, unfortunately, diminishing their relevance accordingly. There are some other suggestive, if not conclusive, characters linking Hupalemur and L. catta. The 4-3-2 sequence of permanent premolar eruption is shared with Lepilemur, and perhaps with indriids as well. A 4-3-2 premolar development sequence, which we did not include as a separate character because of probable correlation with the eruption sequence, has been ascertained with certainty only in Hapalemur and Lemur catta; that sequence does not occur in Lepilemur, although it may be paralleled among indriids. The presence of Wolffian vestiges in the ovary may be another relevant feature there is some doubt about the actual linking Hapalemur and Lemur catta, although distribution of this feature and its consequent polarity. The course of the female urethra could also be a synapomorphy, although if so it is paralleled in Varecia. Thus, in trying to understand the phylogenetics of Lemuridae (minus Lepilemur), we must choose among (1) a genus Lemur comprised of 1,. catta and the L. fuluus-group, for which no shared derived features have been described; (2) a slightly more broadly defined genus Lemur, including Varecia as a contained species, united by the common possession ofa functionally integrated complex ofdental features related to canine honing, and perhaps by facial elongation; or (3) a taxon consisting of Hapalemur and L. catta, linked by a small suite of morphological attributes which are not functionally integrated in any obvious way, but which are echoed by limited evidence from karyology and serology. Obviously we find no reason for choosing the first alternative. If we accept the third choice (which we do), we must somehow explain the long face and canine honing complex shared by L. catta, the L. fulvus-complex, and Varecia. The simplest explanation WC can postulate is a scenario where those characters are synapomorphies of the Lemuridae as a whole, that have undergone a reversal in Hapalemur. In this scenario, secondary reduction of the facial region and elimination of the features associated with a canine hone can be attributed to the increased importance of the upper canine and anterior premolar in the dental processing of Hapalemur’s unique bamboo diet (Milton, 1978). Lemur

Taxonomy

The correct interpretation of the phylogenetic relationships of the Lemuridae pivots on the affinities of Lemur catta. Although one of us (CPG) believes that the evidence that its sister group is the genus Hapalemur is entirely convincing, the second author (RHE) is less

532

C.

convinced

but agrees

we do not espouse On the other pointed

hand,

the

repeatedly

reason purpose

As noted

is not a novel insight

literature.

While

we consider

on our part,

the suggestion

in the light ofavailable

the fulvus-group

of the two mutually

to generic L.

from exclusive

hypothesis.

of the Lemur jihus

of the distinctiveness

This

the rank of theblrulvus-group

of‘opinion,

phylogenetic

doubt

by numerous

authors

(e.g., Groves,

Lemur is L. cattu. For the fulvus-group, 1762. Groves

catta,

without

phylogenetic

but one

of a taxon

evidence,

level. That

author

(1974)

pointed

out

in the last quarter-century

Prosimiu Boddaert, In fact,

there

strategy committing

hypotheses

is

serves the

revolving

that

(1974)

Holthuis

genus

as type

generic

A new generic

name

must

therefore

relevant

sections

in the Appendix;

designation

Nomenclature,

Article

light of the bootstrap

we could

categories

of subfamily

the only used

suprageneric

results

we obtained.

or tribe,

taxonomy

the exclusion

and

International

we do so

( 1912) are

Elliot

Code

(L. B.

has L. cuttu as

for the fulvus-group; (1863),

well

suprafamilial

phylogenetic

insight

neither

ofProsimia,

of Zoological

in various

ways

four genera. Close

to adduce

before

but prefer

taxonomy

is to restrict (1985),

not to combine

these

support

crystallizing

intermediate

& Tattersall

Lepilemur

between

designation.

to do so at present.

to strepsirhine

stronger

of Vareciu

linkage

by introducing

reason

in

relationship

a taxonomic

Like Schwartz

kinship needs

especially

the sister-group

to warrant

we see no compelling

group.

the Lemuridae,

it nor the suggested

supported

does the least violence

for us, but one which able

within we think

of Lepilemur and the Indriidae,

in a formal

been

the

Although

defensible,

to the above

the close affinity

to the group

be provided

with

up the Lemuridae

therefore

Lemuridae

applied

and

this fixation

69(a). to alter

split

that

(1912),

not affect

can verify that Lemur cattu is the type species

is sufficiently

Although

have

(1978),

generically,

to use Prosimiu. Lemur cattu

wrong

( 1785), Gray

in accordance

of L. cutta to Hapulemur is eminently the fulvus-group

name

Boddaert

the reader

by subsequent

We see no reason

from

were

( 1870) does

other

quoted

Tattersall)

for nomenclatural

1785. Von Hagen

of Prosimia by Elliot

Every

The

the family

(1978)

species

in litt.).

below.

The course

of

Prosimiu Brisson,

the subgenus

is unavailable

L. cattu and the fulvus-group

cattu by Gray

of the species

to CPG,

type species.

work

from Boddaert

to separate

and von Hagen

1758, was fixed

this

assigned

Brisson’s

1983,) the type species

1785 for the latter.

Groves

Linnaeus,

1974; Tattersall,

Hill (1953)

but that Prosimia is available

purposes,

admit

this difference

L. cuttu.

around

and

Given

our preferred

to L. c&a.

of dissociating to either

t.XGLt.N

can be little

in the

for elevating

nomenclature

from

reflecting

Hupalemur and L. cattu to be premature

containing ample

there

H.

K.

is reasonable.

changes

in comparison

out

AND

that this interpretation

nomenclatural

species-complex

tiKVVtS

k’.

and

indriids

is a

than we (or Schwartz

it in the language

nomenclature. We are prepared to suggest nomenclatural change taxon in a 95% confidence interval by the bootstrap procedure.

we taxa

when

&

of zoological

we can place

the

Generic diagnoses Lemur Linnaeus, Synonyms:

Prosimiu Brisson,

1785; Catta Link,

1806; Maki Muirhead,

1895; Odorlemur Bolwig, 1960. Diagnosis: The genus Lemur is unique with alternating

1758 P rocebus Storr,

1762 (unavailable);

1780; Prosimia

1819; Mococo Trouessart, among

black and gray annulations;

the Lemuridae wholly

glandular,

Boddaert,

1878; Eulemur Haeckel,

in the following glabrous

features:

scrotum;

length

tail of

LEMURID

facial

skeleton

more

cling

to their

mother’s

than

50%

of total

Vurecia in the more

or less parallel

medial

although

pterygoids,

shares

a canine

lower anterior and

honing

develop

indriids);

Wolffian

presence

of brachial

and Ha/demur, at the distal Contained

erupt

fundus

persist

in the ovary. glands,

L. cutta Linnaeus,

Diagnosis:

The genus

upper

and

due

Hapalemur

lower

soon clings

to its mother’s

at least,

(as among

also

and

be true

in

a fovea-like Like Vurecia

bulla.

Link,

Standing,

urethra

opens

(Elliot,

1912).

This

genus

are placed

penile

structure

than

other

among

lemurids

Petterus in reduction

for the talonid

basin

the

V. variegata Kerr,

species:

Synonyms:

Prosimia of various

but

under

H.

that genus.

not H. griseus,

1871

Hapalemur

(synonym

of the

1851) H. griseus.

St. Hilaire,

1863 orally

(approx.

in the period

described premolar,

is extremely

typically

short

for its

sac is present.

for those

genera

and in lacking

Lepilemur in the latter).

The

above.

It

any lingual

Like Petterus it shows

but in Vurecia it is more

1792; type by monotypy

characters:

the female

3.2 kg); a throat

upper molar,

following

by the mother;

the gestation

(it also resembles

Contained

listed

the

after birth,

H. simus, but

Lemuridae

in the features

upper

is absent, shows

on the neck.

(I. Gcoffroy

of the anterior

in the size of the posterior

mechanism the baculum

immediately

spines.

characters: paroccipital

[ 19761 and Vuillaume-Randriamananthere is a need to reconsider the status

per litter;

Lemur and Hapalemur

resembles

orally

the

MahP

(we believe

offspring

honing

H. simus Gray,

1795;

in a nest and transported

to two or three

in the following molariform;

the Lemuridae;

is carried

by monotypy

is unique

1851

1905.

Lemur in the features

1905-see

others

designation

a canine

within

the neonate

H. griseus

gallieni

size; it is larger

reduction

tapering

Lcmuridae

Vurecia Gray,

outlet

may

exhibits

and the female

distinctly

indriids);

a glandular

of H. griseus). Type

Diagnosis:

resembles

canine

with both Petterus

H. griseus and H. simus in the

St. Hilaire, Standing,

Vurecia in lacking

tena ef al. 119851); perhaps

genus

(this

the retina

foramcn,

are

fur. It resembles

resembles

species:

[Prohapalemur]

body

and

among

reversal

bifurcation;

Vurecia in having

Contained

gives birth

and genus

with Hapalemur griseus: permanent sequence

It resembles

I. Geoffroy

premolars

to an evolutionary

of a distal

Neonates

to the upper

1758; type by subsequent

is unique

posterior

beginnings

subspecies

distal

and a posteriorly

187 1; Prohapalemur

is long and blade-like

resembles

The

end of the clitoris.

Hupalemur

griseus,

resembles

the presphenoid constricted.

lower premolar,

characters

pigmented.

The genus

is more

diastemata

derived

and antebrachial

Prolemur Gray,

process

between

it has a very large zygomaticofacial

species:

perhaps

of the sutures presphenoid

in a postero-anterior is spottily

vestiges

Synonyms: The

indriids.

including

the following

the ocular

in some

and a wear facet on the anterior

and

structure;

direction

Petterus in that neonates

It resembles

also occurs

in Lemur the

mechanism,

premolar,

Varecia. It shares

premolars

skull length.

fur; this feature

533

SYSTEMATICS

(Gray,

pronounced.

1863).

Petterus gen. nav. 1978); not of Boddaert, Diagnosis: The genus The paranasal interorbital

(Gray,

1863; Hill,

1953; Groves,

1785 (= Lemur Linnaeus, 1758). Petterus is unique among the Lemuridae

air sinuses, region

authors

projects

especially above

the palatine the plane

in the following

and presphenoidal,

of the remainder

1974; von Hagen,

are much

features: dilated;

of the skull roof, creating

the a

534

C. P.

GROVES

AND R. H. EAGLEN

bubble-like effect in its cranial profile; relatively robust pericones occur on the anterior upper molars, especially Ml; the posterior upper molar is somewhat smaller than the middle (a more pronounced condition occurs in I’urecia); it possesses a few small penile spines. For features in which it resembles other lemurids, see the preceding diagnoses. Contained species: P. jidvus E. Geoffroy, 1796; P. macaco Linnaeus, 1766; P. mongoz Linnaeus, 1766; P. coronatus Gray, 1862; P. rubriventer I. Geoffroy St. Hilaire, 1850; probably others. Type species: Petterus fulvus. Etymology: to honor Dr. Jean-Jacques Petter, who since the late 1950s has come to personify the scientific study of Malagasy lemurs; has inspired his students and colleagues with his intense interest in and love of lemurs; and has strenuously promoted the conservation of the Malagasy fauna. We feel that it is high time that this remarkable scientist’s contributions to primatology and conservation are recognized nomenclatorially, and are delighted at having the opportunity to do so. We thank Bill Jungers for his suggestion as to the appropriate form of this name.

Acknowledgements We wish to express our sincere thanks to the curators and curatorial staffs of the various museums which provided us access to their specimens. Special thanks are due to Matt Cartmill, who provided wet specimens for dissection of the facial region. The Computation Center of the University of Puerto Rico Medical School provided computer time, while Joe Felsenstein, David Swofford, and Jim Rohlf provided the computer programs to implement the quantitative analyses. Warren Hudson receives our gratitude for doing the photography, as do the reviewers of this manuscript, anonymous and otherwise, for their suggestions to make it better. References R. J. (1964). The displays of primates. In (J. Buettner-Janusch, Ed.) Evolutiomzry and Genetic Biology of Vol. 2, pp. 227-309. New York: Academic Press. Andriamiandra, A. (1972). L’appareil genital femelle du L~murcatta Linnaeus 1758: histologie et histophysiologie. Bull. Assoc. Anatomistes 155, 163-181. Barnicot, N. A. & Hewett-Emmett, D. (1974). Electrophoretic studies on prosimian blood proteins. In (R. D. Martin, G. A. Doyle & A. Walker, Eds) Prosimian Biology, pp. 891-902. London: Duckworth. Boddaert, P. (1785). Elenchus Animalium, Vol. 1. Rotterdam: C. R. Hake. Bolwig, N. (1960). A comparative study of the behaviour of various lemurs. M&. de /‘Inst. Sci. de Madagascar 14 (Sk. A), 205-217. Buettner-Janusch, J, & Buettner-Janusch, V. (1964). Hemoglobins of primates. In u. Buettner-Janusch, Ed.) Evolutionary and Genetic Biology of Primates, Vol. 2, pp. 75-90. New York: Academic Press. Dene, H. & Goodman, M. (1978). Immunodiffusion investigations of the systematics of Lemuridae. Paper presented at 2nd annual meeting of American Society of Primatologists, Atlanta, Georgia, September 69, 1978. Dene, H.. Goodman, M. & Prychodko, W. (1976). Immunodiffusion evidence on the phylogeny of the primates. In (M. Goodman & R. E. Tashian, Eds) Molecular Anthropology, pp. 171-195. New York: Plenum Press. Eaglen, R. H. (1980). The systematics of living Strepsirhini, with special reference to the Lemuridae. Ph.D. Dissertation, Duke University. Eaglen, R. H. (1983) Parallelism, parsimony, and the phylogeny of the Lemuridae. Int. J. Primatol. 4, 24%273. Eaglen, R. H. (1986). Morphometrics of the anterior dentition in strepsirhine primates. Am.]. phJ$. Anlhrop. 71, 185-201. Elliot, D. G. (1912). A Review ofthe Primates. Monograph No. 1. New York: American Museum of Natural History. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evol. 39, 783-791. Fiedler, W. (1956). Ubersicht fiber das System der Primates. In Primatologia, Vol. I, pp. l-266. Basel: Karger.

Andrew,

Primates,

LEMURID

535

SYSTEMATIC3

Gazin, C. L. (1958). A review ofthe Middle and Upper Eocene primates ofNorth America. Smithsonian Misc. Co/l. 136, l-l 12. Gray, J. E. (1863). Revision of the species of lemuroid animals, with the description of some new species. Proc. Zool. Sot. London 1863, 129-152. Gray, J. E. (1870). Cataloguc of Monkeys, Lemurs, and Fruit-eating Bats in the Collection of the British Museum. London: British Museum (Natural History). Gregory, W. K. (1920). On the structure and relationships ofNotharctus, an American Eocene primate. Mem. Am. MUX. nat. Hist. n.s. 3, 49-243. Groves, C. P. (1974). Taxonomy and phylogeny of prosimians. In (R. D. Martin, G. A. Doyle & A. C. Walker, Eds) Prosimian Biology, pp. 435-448. London: Duckworth. Hill, W. C. 0. (1953). Primates: Comparative Anatomy and Taxonomy. Volume I: Strepsirhini. Edinburgh: The University Press. Jolly, A. (1966). Lemur Behavior. Chicago: University of Chicago Press. Jouffroy, F. K. & Lessertisseur, J, (1959). La main des Ltmuriens malgaches comparee a celle des autrc Primates. Mim. de l’lnrt. Sci. Madagascar 13 (Ser. A), 195219. Mahe, J. (1976). Craniometrie des Itmuriens: analyses multivariables-phylogenie. Mim. Mus. nat. Hilt. nut. Paris (C) 32,

Maier,

l-342.

W. (1980).

naturforsch.

Matthew,

Konstruktionsmorphologische

Ges. 538,

Studien

am Gebiss

der rezenten

Prosimiae.

Abk. senckenb.

l-158.

W. D. (1909). The Carnivora

of the Bridger Basin, Middle Eocene. Mem. Amer. MU.

and Insectivora

nat. Hirt. 9, 289567.

Milton, K. (1978). Role of the upper canine and Ps in increasing the harvesting efficiency ofHapalemurgriseus Link 1795. J. Mumm. 59, 188-190. Napier, J. R. Napier, P. H. (1967). A Handbook ofLiuing Primates. New York: Academic Press. Olson, T. R. (1979). Studies on aspects of the morphology and systematics of the genus Otolemur Coquerel, 1859 (Primates, Galagidae) Ph.D. D’tssertation, University of London. Oxnard. C. E. (1971). Tensile forces in skeletal structures. 1. Morbh. 134, 425-436. Pariente, G. (1970). ‘Retinographies comparees des LPmur:ens malgaches. C. R. Acad. Sci. Hebd. (Paris) 270, 1404-1407. Petter, J.-J. (1965). The lemurs of Madagascar. In (I. DeVore, Ed.) Primate Behauior, pp. 292-319. New York: Holt, Rinehart, & Winston. Petter, J.-J., Albignac, R. & Rumpler, Y. (1977). Faune de Madagascar: Lemurienr. Paris: Centre Nationale de la Recherche Scientifique. Pocock, R. I. (1918). On the external characters ofthe lemurs and of Tarsius. Proc. Zool. Sot. London 1918, 19-53. Rumpler, Y., (1975). The significance of chromosomal studies in the systematics of the Malagasy lemurs. In (I. Tattersall & R. W. Sussman, Eds) temur Biology, pp. 2540. New York: Plenum Press. Rumpler, Y. & Andriamiandra, A. (1971). Etude histologique des glandes de marquage du cou des Lemuriens malgaches. C. R. Sot. Biof. 165,436441. Rumpler, Y. & Dutrillaux, B. (1978). Chromosomal evolution in Malagasy lemurs. III. Chromosome banding studies in the genus Hapalemur and the species Lemur catta. Cytogcnct. Cell Genet. 21, 201-211. Rumpler, Y. & Dutrillaux, B. (1986). Evolution chromosomique des Prosimiens. Mammalia 50, 82-107. Sarich, V. M. & Cronin, J. E. (1976). Molecular systematics of the primates. In (M. Goodman & R. E. Tashian, Eds) Molecular Anthropology, pp. 141-I 70. New York: Plenum Press. Schwartz, J. H. & Tattersall, I. (1985). Evolutionary relationships of living lemurs and lorises (Mammaha, Primates) and their potential.afIinities with European Eocene Adapidae. Anthrop. Papers. Amer. Mus. nat. Hist. 60, l-100. Seligsohn, D. (1977). Analysis ofspecies-specific molar adaptations in strepsirhine Primates. Contrib. Primatol. 11, l-l 16. Simpson, G. G. (1945). The principles ofclassiiication and a classification ofmammals. Bull. Amer. Mus. nat. Hist. I

85,

.

II

I

I-350.

Sneath, P. H. A. & Sokal, R. R. (1973). Numerical Taxonomy. San Francisco: Freeman. Swofford, D. L. (1985). PA UP: Phylogenetic Analysis CTing Parsimony, version 2.4. Champaign, Ill.: Illinois Natural History Survey. Szalay, F. S. & Delson, E. (1979). Euolutionary History ofthe Primates. New York: Academic Press. Tattersall, I. (1983). The Primates of Madagascar. New York: Columbia University Press. Tattersall, I. & Schwartz, J. H. (1974). Craniodental morphology and the systematics of the Malagasy lemurs (Primates, Prosimii). Anthrop. Papers Amer. MU. nat. Hist. 52, 139192. Von Hagen, H.-O. f 1978). Zur Verwandtschaft der “Echten Makis” (Prosimii, gattung Lemur). Zool. Beitriige 24, 91-122.

Vuillaume-Randriamanantena (Prohapafemur)

gallieni

L. R. & Sutherland, M., Godfrey, (Standing, 1905). Fotia primatol. 45, 89116.

M. R. (1985).

Revision

of Hapalemur

C. P. GROVES

536

AND

R. H. EACLEK

Appendix of Prosimia is here reproduced

The literature with

the International

Code

Lemur catta, and that

the name

1. Prosimia Boddaert, II.

in outline

of Zoological

in order

Nomenclature,

is accordingly

to show that, in accordance

Article

not available

1, 43. The text reads

Elenchus Animalium,

69, the type

species

is

for the fuluus-group. as follows:

(Lemur Linn.).

PROSIMIA CAPUT:

rostrum elongatum;

Dentes

superiores

aures penduli.

vulpinum,

IV.

intermediis

antici

longiores.

remotis

inferiores

VI.

longiores

compressi

approximati. Laniarii

solitarii.

Molares sublobati

Mammae quattuor

pilosum,

CORPUS

PEDES: femora

(Approximate

posteriora

muzzle

Upper

teeth

elongated;

single.

Molars

sublobate, hairy,

“II.”

in front Genus

four,

“pendulous”

VI, very long,

pectoral;

(probably

of Prosimia

tail long, means

indicates

I is Simia; genus IV is Bradypus;

genus

ears

teeth

(probably

means

compressed

“free”).

together.

very long. “thighs”

FEET: posterior

Briss.);

front

mammae

Quadrumania.

fox-like,

IV. Lower

Canines

Prosimia

pilosa.

translation:

HEAD:

BODY

The

cauda longa,

pectorales;

plantae manuformcs.

longiora,

that

III

hairy.

limbs) this

very long, feet hand-like.)

is the

is Tardigradus

second

(with

V, Vespertilio; VI,

genus

synonymy

Dasypus; VII,

of the

order

Lemur Linn.,

Manis; and VIII,

Myrmecophaga. The genera (with

a very

are listed slightly

again

further

different

on, this time with

characterization)

macaco, catta, volans, spectrum, minima. (The first three same

names;

The genus

the fourth

is the Colugo;

Tardigradus contains

Quadrumania

contain

species

their

includes

contained

species.

the following

are the species

the fifth, the Tarsier;

known

the sixth

today

mongoz, under

the

is a Mouse-Lemur.)

the two species

loris and coucang. The remaining

today

to the orders

Chiroptera,

13 1. In Gray’s

family

assigned

Prosimia

species:

genera

Edentata,

of and

Pholidota. 2. Prosimia Gray, two informal and Prosimia.

This

PROSIMIA. Head

Further

Proc. Zool. Sot. London, 1863,

sections:

on (pp.

Indrinina

last is defined without

and Lemurina.

The latter

the following

hairy;

10 species

wrist

are allocated

to Prosimia:

mongoz, ruJifron.s, xanthomystax, coronata, albimana,

(These

of the&lvus-group

are all members

as recognized

here.)

albifrons,

anjuanensis, collaris.

On p. 136, the species

catta

to Lemur as its only species.

3. The type designations to Primates,

are

hairy.

nigrifrons, melanocephala, is assigned

there

Vurecia, Lemur,

as follows:

any ruE, ears externally

137-139),

Lemuridae

has three genera:

he states

( 19 12). On p. xxviii,

listing

the generic

names

applied

baldly:

1758. LEMUR Linnaeus, 1762. PROSIMIA Brisson, 1780. PROCEBUS

of Elliot

Storr,

Syst. Natur., pp. 29, 30. Type Lemur catta Linnaeus. Regn. Anim., pp. 13, 156-158. Type Lemur catta Linnaeus. Prodr.

Method.

Mamm.,

pp. 32, 33. Type

Lemur catta Linnaeus.

LEMURID

-and

so on. Later

on (pp.

Lemur as recognized

131-139)

by him.

he gives

a “Literature

of the Species”

of the genus

of Prosimia:

On p. 132 he treats

Brisson, Regnum Animale. Four species of LEMUR are here given,

1762.

537

SYSTEMATICS

under

Prosimia: viz., P.&sca,

the genus

pedibus albus, P. pedibus fulvis, and P. cauda annulis cincta. The first three determined LEMUR

Boddaert There

are some

the

aspects

work,

(non-binomial)

Be that

Gray’s

as it may,

failure

than

there

is without

doubt genus. places

went

on in those

his Tardigradus;

under

Article

69. Type

the provisions

and

the

other

in error. errors

in

Prosimia Briss.”

and that his failure

a form

of plagiarism

Prosimia is not truly a homonym

Boddaert’s

to cite any of in the modern Prosimia

of Brisson’s

for his Prosimia is! again,

authority

it would

is absolutely which

species

was established

days,

way to

is clearly

to give “Lemur Linn.,

meant

does not cite

in his telegraphic

name. than

69 of the Code,

that Boddaert

but seems

to his own Tardigradus-which

no doubt states

that

Elliot’s

in

repeated

in two places,

of

fulfills

the criteria

of

as follows: publication.-If

193 1 and no type species

of this Article

action,

(recte Prosimia Boddaert)

not fixed in the original

before

less surprising

be today.

L. catta the type of “Prosimia Brisson”

article

It is curious

at all is not simply

to give any previous

of its times

Finally, making

however,

as the type of Brisson’s are listed in the appropriate

Prosimia,

that Boddaert

species

of the same

the context

that

“lifting”

it is possible

his own Prosimia rather

but a usage

works.

genus

Prosimia is equivalent

widespread

Brisson’s sense.

the fourth,

be regarded

but his names

of these

of his (Boddaert’s)

that Brisson’s

Boddaert’s

taxon

in this section,

curious

in respect

under

of certainty,

and must

be

synonymies.

Brisson Given

Linnaeus

is not mentioned

in species

imply

with any degree

CATTA

P.

cannot

apply

subject,

when

a nominal

genus-group

was fixed in the original

appropriate,

publication,

to the provisions

of Article

70b. c. (a)

Subsequent

species

included

nominal

of that nominal designation

genus

70b, c refer to misidentified

(1) If no nominal established,

species

the nominal nominal

Subsection

the unavailable

could

ADDED

IN

in manuscript,

This

proposal

genus

or subgenus

designates

validly

(type by subsequent

but

one of the

designates

the type

designation),

and no

or misapplied possibly

was included species

type species, appropriate

and so are irrelevant

is [i] [l],

at the time the nominal

that were first and subsequently to in the Subsection

are deemed

which

genus

here.

states:

or subgenus

and expressly

was

included

to be the only originally

species. be taken

Brisson

paper

(see [i] to [iv] below)

or subgenus

mentioned,

in it in any of the ways referred included

a nominal

who subsequently

is valid.

Of the “[i] to [iv] below”

NOTE

established

originally later

This

author

the first author

species

Article

designation.-Ifan

did not fix its type species,

treats

as referring

to the available PROOF:

Tattersall

proposed

to designate

Brisson’s

and

to the transfer

Boddaert, (1988)

of authorship

but seems has

recently,

of Prosimia from

not to be strictly after

seeing

necessary. the present

mongop as the type of Prosimia Boddaert,

Boddaert’s

usages

of Prosimia

as

if they

1785. were

538

C.

P.

GROVES

AND

R.

H.

EAGLEN

independent. They are not. The decisive passage in the Code of Zoological (1985) is a follows:

Nomenclature

“Art. 67 (f). Incorrect citations.-If, in designating the type species for a nominal genus or subgenus, a subsequent author attributes the name of. . . the genus or subgenus to an author or date other than that denoting its first establishment . . . he or she is nevertheless to be considered, if the nominal species was otherwise eligible, to have validly designated the type species.” In the present instance, quoting a wrong author and date (Brisson instead of Boddaert, if Brisson is indeed deemed to be unavailable as is generally taken to be the case [though it has not in fact been so ruled by the Commission]) does not invalidate Elliot’s fixation. Elliot’s designation of cutta as type species of Prosimia therefore stands, and Tattersall’s attempt to overturn it is invalid, being based on a misunderstanding. As before, we thank Prof. L. B. Holthuis for drawing our attention to the relevant section of the Code, which, as he notes, is quite clear on this point. Tattersall,

I. 1988. A note on nomenclature

in Lemuridae.

Phys. Anthrop. News 7 (l),

14.