Bwlagkaljoumal afth Linnean Sociep (1997), 62: 383400. With 7 figures
How the leopard got its spots: a phylogenetic
view of the evolution of felid coat patterns
LARS WERDELIN
Department of Palaeozoology, Swedish Museum
S-104 05 Stockholm, Sweden
ofNatural History, Box 50007,
LENNART OLSSON
Department of Environmental and Developmental Biology, Uppsala Uniuersi& Norbyuijgen 18,
S-52 36 Uppsala, Sweden
Received 18 October 1996;acceptedfor publication 15 May 1997
The current theory of felid coat pattern evolution proposes that the primitive pattern is one
of relatively large spots that break down into smaller spots (here denoted flecks) and rosettes
while at the same time leading to various striped patterns as sidelines. We have coded the
coat patterns of felids into uniform, flecks, rosettes, vertical stripes, small blotches and blotches
and show by mapping these character states onto phylogenies of the family that the current
theory is flawed. Instead, the primitive pattern appears to be flecks and it is from this type
that nearly all other types have developed. The robustness of this hypothesis is shown by
the fact that it remains unchanged regardless of which of several quite Merent, competing
phylogenies of the family is used. The pattern of transformations reconstructed is not
predicted by current theories of pattern formation and we suggest that modellers pay closer
attention to the phylogenetic histories of the features that they model.
0 1997 The Linnean Society of London
ADDITIONAL KEY WORDS:-Carnivora - Felidae - coat pattern -phylogeny
- modelling.
-
evolution
CONTENTS
Introduction . . .
The present theory
Felid phylogeny . .
Character coding .
Species . . .
Character evolution
Discussion . . .
Conclusions . . .
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384
384
386
386
389
392
397
399
Correspondence to Dr L. Werdelin. email: [email protected]
00244066/97/110383
+ 18 $25.00/0/bj970147
383
0 1997 The Linnean Society of London
L. WERDELIN AND L. OLSSON
384
Acknowledgements
References . . .
. . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . .
399
400
INTRODUCTION
The developmental biology and adaptive value of coat patterns in mammals has
generated a great deal of interest in recent years (Murray, 1981b, 1988; Godfrey,
Lythgoe & Rumball, 1987; Ortolani & Caro, 1996), This is especially true of the
coat patterns of cats, family Felidae, which have fascinated humans for centuries
because of their intrinsic beauty and great variability. Despite this, there have been
very few studies that have considered the evolutionary history of these patterns.
This may be due both to the difficulty of ascribing them to a specific developmental
mechanism and to the apparently untestable nature of hypotheses regarding the
history of features that do not fossilize.
With the advent of cladistic methods of phylogenetic inference it has become
possible to reconstruct historical events in a phylogenetic framework, and also to
reconstruct past changes in characters on the basis of a hypothesis of relationships
between extant and/or fossil taxa sharing these characters. By reconstructing past
changes we can test existing hypotheses of character change, and either confirm
that they are consistent with our phylogenetic inferences, or reject them and replace
them with an alternative based on current phylogenetic knowledge.
In this paper we shall attempt to infer the origin and evolution of felid coat
patterns on the basis of current ideas regarding felid phylogeny. We will test and
reject the currently accepted theory and replace it with one which has its basis in
the phylogeny of the Felidae. We will also briefly discuss some current models for
the development of felid coat patterns in the light of the phylogenetic inferences
made.
THE PRESENT THEORY
Much has been written about the coat patterns and coat pattern variahon of
various felid species (e.g. Pocock, 1910; Hemmer, 1967; Mohr, 1967; Peters, 1982),
but there exists only one hypothesis for their evolution that encompasses the entire
family: that of Weigel (1961). This hypothesis has been commonly cited in the
general literature (Ewer, 1973; Kitchener, 1991), but its structure is not at all clear.
Basically, Weigel’s proposal, backed by a figure (Weigel, 1961, fig. 24; see Fig. 1) is
that the primitive pattern for felids is one of relatively large spots which have a
tendency to bre& d m , first by developing a lighter centre and then by breaking
up into smaller spots spaced into rosettes and later individually. At each step in this
general decay of the basic pattern striped patterns may develop.
Several points about this hypothesis are unclear. First of all, there is no indication
in the text of how the author arrived at the hypothetical primitive pattern. The
remainder of the theory is based on developmental data and on comparisons
between closely related taxa. The theory is explicitly stated to be phylogenetic
(‘stammesgeschichth’), however, so something besides these criteria is implied. In
the absence of a specified primitive felid group, we are unable to say what these
additional criteria might be. Accordingly, we will here accept Weigel’s hypothesis
as it is expressed in Figure 1.
FEUD COAT PATTERNS
385
t
t
t
uniform
Figure 1. The current hypothesis of coat pattern evolution in Felidae. After Weigel (1 961, fig. 24).
We propose to test Weigel's theory by parsimoniously mapping a qualitative
coding of the coat patterns of modern felids on cladograms expressing current views
of felid phylogeny. In so doing we can reconstruct the changes in state which can
be inferred to have occurred in the history of felids and compare these historical
changes with the ones hypothesized by Weigel (196 1) to have occurred.
We can also use the reconstructed history to examine some predictions generated
by current models of the development of coat patterns in mammals. The dominant
approach to mathematical modelling of mammalian coat patterns has been to use
Turing type reaction-diffusion mechanisms (Turing, 1952; Murray, 1981a, b, 1993).
In these models a prepattern is formed by dfising morphogens (often an activator
and an inhibitor). This prepattern is then reflected in the actual coat pattern of the
animal. It has been suggested that a single mechanism can produce all mammalian
coat patterns (Murray, 198la, b). An important prediction generated by this approach
is that the size and shape of the animal at the time when the pattern formation
mechanism operates is crucial for determining the pattern.
The models have usually been designed without taking the phylogenetic component
into account and questions such as whether a specific transformation series is
produced when some parameter is changed are seldom adressed. We hope that our
work can stimulate thoughts in this direction.
386
L. WERDELIN AND L. OLSSON
FEUD PHYLOGENY
In order to carry out the analysis we must have a hypothesis of felid interrelationships. Unfortunately, this is a contentious field, but we shall see how we
can turn this debate to our advantage in the analysis of coat pattern evolution.
There are several competing phylogenies of the Felidae available at the present
time. These phylogenies have been developed using different character sets and
different methods of phylogeny reconstruction and are therefore not directly comparable.
The first phylogeny we shall consider is that of Herrington (1986).This phylogeny
(Fig. 2A) is based mainly on a literature study of characters of the skeleton and soft
anatomy. It is not based on a maximum parsimony analysis of the characters, but
is instead a somewhat subjective assessment of character state distributions. For this
reason among others it is 9 e only fully resolved of the phylogenies discussed herein.
The second phylogeny (Fig. 2B) was presented by Collier & O’Brien (1985) and
is based on immunological distance data. This is a very attractive hypothesis of
interrelationships, but suffers from the usual problems of distance data, especially
that the nodes cannot be related to specific characters or character states.
The most recent phylogeny of the Felidae is the work of Salles (1992). This
phylogeny is the result of a maximum parsimony analysis of characters of the skull
and dentition. It is notable not least for its many differences from that of Collier &
O’Brien (1985) (Fig. 2B). Since Salles (1 992) is the only one of the aforementioned
authors to provide a full data matrix we have had the opportunity of reanalysing
his data with some interesting results. The most important aspect of this reanalysis
is that it shows that the results presented by Salles (1 992) do not represent the most
parsimonious solution for this data matrix. Instead of 409 trees of length 157 as
reported for the full 57 character matrix we found 466 trees of length 155 (using
PAUP 3.1.1; Swofford, 1990). Using the same procedure of successive weighting as
Salles (1992) we brought this total down to 45 trees, the strict consensus tree of
which is seen in Figure 3.
Topological differences between this tree and that published by Salles are
substantial in some areas. Lptuilums s m a l is moved from a sister group relationship
with Prionailurus bengahis to one with the Felis group. The species of the Lobardus
group of South American cats are moved into close proximity to each other (although
they have not been rendered monophyletic), along with Rionailurus rubiginosus and
R bengalensis. pfofelistrmminckii, R badia, and Pardofelis marmoratu form a monophyletic
group instead of a paraphyletic one as in Salles’results. Finally, the basal relationships
within the family are poorly resolved. However, the mapping of coat pattern
character states showed that the previously published version of this phylogeny
(Salles, 1992) and our revised version indicate identical state transformations in the
evolution of coat patterns and we therefore do not here figure Salles’ (1992) original
version.
In the following analysis we shall use this revised phylogeny (Fig. 3) to exemplify
how the character mapping procedure was carried out.
CHARACTER CODING
The character analysis and coding is the most complex aspect of a phylogenetic
analysis, especially in cases such as the present one, where there is a great deal of
FELID COAT PATTERNS
387
A
B
Figure 2. Two currently available hypotheses of felid interrelationships.A, the phylogeny of Herrington
(1 986). B, the phylogeny of Collier & O’Brien (1 985) displayed in cladogram form.
intraspecilic variability to consider and where character states tend to intergrade
with each other. We have decided to code felid coat patterns into six discrete
categories: flecks (small spots not organized into patterns), rosettes (small spots
organized into patterns of six or fewer spots), small blotches (small irregularly shaped
388
L. WERDELIN AND L. OLSSON
Figure 3. The phylogeny we obtained from Salles’ (1992)data. This phylogeny examplifies the mapping
procedure used to analyse coat pattern evolution. Each species is given a character state code and the
ancestral conditions are reconstructed parsimoniously by a computer algorithm (Maddison & Maddison,
1992). The changes from one character state to another in the phylogenetic history of the group can
then be extracted (Fig. 5).
areas of dark on a usually lighter background), blotches (large areas of variable
colour framed by dark and set on a lighter background), vertical stripes (dark,
dorsoventrally or anterodorsally-posteroventrallydirected stripes on a lighter background), and uniform (no distinguishable pattern) (Table 1 and Fig. 4).In tables
and diagrams these are coded flecks = 0, rosettes = 1, small blotches = 2, blotches =
3, vertical stripes =4,uniform = 5 . These six types were chosen because, although
intergradable, they are readily distinguishable as types, and the basic pattern of
each species of extant felid can be referred to one of the types. If less than six types
had been chosen it would have been difficult to code all species consistently and if
the subdivision had been finer the end result would have been of limited value, as
general patterns would have been difficult to discern.
In the coding we have paid much attention to the juvenile coat patterns of the
species (where known), since we believe that in most cases the juvenile patterns
represent the more general (‘primitive’) condition for the species, whereas adult
patterns to a greater extent are influenced by adaptations to hunting behaviour and
other characteristics of the species (cf. Ortolani & Caro, 1996).The obvious exception
to this dictum is the cheetah (Acinonyx jubatm), in which the juvenile coat is very
different from both the addlt cheetah and all other juvenile felids in being less
distinctly spotted than the adult and having a ‘rug) of long, lighter-coloured hairs
on the back. Presumably this coat pattern improves crypsis of the young in the
cheetah’s chosen habitat and has sometimes been suggested to mimic the coat
pattern of the honey badger (Mellivora capensis), an aggressive mustelid with which
the cheetah is partially sympatric (Eaton, 1976).
FELID COAT PATTERNS
389
TABLE
1. The coat patterns of all living felid species as coded in this paper, along
with an approximate head+body length for each species. (Data from various
literature sources)
+body length (mm)
Species
Coat pattern
Head
I! Leo
P pardus
I? onca
Rtiglis
F! uncia
JV nebulosa
F! marmorata
L. bnx
L. canadmis
L. pardinus
L. m l
A jubatus
H . yagouamndi
F! concolor
L. serual
C. caracal
F! bmgalensis
F! m'veninus
F! phniceps
F! mbinosur
F! kmminckii
F! aurata
F! badia
R bbica
R caja
R bicti
R silveshir
R matganta
R nignpes
E chaw
0. manul
L. pardab
L. wiedii
L. tgrinur
L. colcolo
L. geofiyi
L. guigna
0.jacobitus
Rosettes (uniform as adult)
Rosettes
Rosettes
Vertical stripes
Rosettes
Blotches
Blotches
Flecks
Flecks
Flecks
Flecks
Flecks (mottled in king cheetah)
Uniform
Flecks (uniform as adult)
Flecks
Uniform
Flecks
Flecks
Uniform
Flecks
Polymorphic
Flecks (variable as adult)
Uniform
Vertical stripes
Vertical stripes
Vertical stripes
Vertical stripes
Vertical stripes
Flecks
Vertical stripes (uniform as adult)
Vertical stripes
Small blotches
Small blotches
Small blotches
Polymorphic
Flecks
Flecks
Vertical stripes
1400-2500
910-1910
1220-1850
1 190-2800
990-1300
620-1070
450610
800- 1300
800- 1000
850-1 100
651-1250
I 040- 1450
510-770
970-1960
670- 1000
600-1050
440-1070
650-860
410610
350-480
730- 1050
620-1020
500490
434-660
460665
685-853
400-750
390-579
337-500
500-853
500-650
550-1000
463-790
400-550
567-700
450-700
390-5 10
570640
Species
Puntheru leo, lion. The adult lion has a more or less uniformly coloured coat. The
juveniles, however, are patterned with flecks, and these flecks can persist in some
adult individuals, especially on the legs and belly. It is also clear from good
illustrations ofjuvenile lions (Seidensticker, 1991: 223) that the flecks are laid down
as rosettes, as in other spotted Punthu.
Puntheru pardus, leopard. There is no doubt that leopards have flecks that are laid
down as rosettes.
Puntheru oncu, jaguar. The coat has flecks laid down as rosettes.
Puntheru tigris, tiger. The coat is marked by vertical stripes. Various colour variations
are known, as are patterns apparently due to developmental anomalies, but no true
spotted tigers are known.
390
L. WERDELIN AND L. OLSSON
Figure 4. The six different coat patterns we have used in coding all living species of felid. k f t column,
top to bottom, flecks, rosettes, vertical stripes; right column, top to bottom, small blotches, blotches,
uniform.
Panthera uncia, snow leopard. This species also has flecks laid down in rosettes,
although the rosettes are less distinct and tend to run together into rings.
fleojielis nebulosa, clouded leopard. The coat of this species defines what we mean by
blotches. It is made up of large fields of dark fur with an even darker frame,
separated by narrow bands of lighter fur.
Pardofelis mamorata, marbled cat. The coat of this species looks very much like a
smaller version of the coat of the clouded leopard, and we consider it blotched.
Lynx bnx, Eurasian lynx. The coat of this species is clearly marked with flecks. In
northern populations these are less distinct than in more southerly ones.
Qnx canadensir, Canada lynx. This species has a coat very similar to the closely
related Eurasian lynx, but the flecks are even less distinct.
Lynx pardinus, Iberian lynx. A species that has a coat that is very distinctly marked
with flecks.
Lynx m f i , bobcat. Like the Eurasian lynx, this species has a variable coat pattern
made up of more or less distinct flecks depending on the population.
Acinonyx jubatus, cheetah. Has a coat with distinct flecks. The deviant king cheetah
is the effect of a simple mutation (Van Aarde & Van Dyk, 1986)
Herpailurn yaguarondi, jaguarundi. This species is apparently entirely uniformly
coloured, the only exceptions being lighter areas around the snout and eyes. Although
Weigel (1961: 53) mentions that the eyra colour phase (see below) has reddish spots
on the belly we have been unable to confirm this. There are no data available in
the literature on the juvenile coat of this species. The two colour variants, the eyra
(reddish brown) and the jaguarundi (silver grey) are well known and depend on the
presence of eumelanin or phaeomelanin.
Puma concolor, puma, mountain lion, cougar. Like the lion this species is uniformly
coloured as an adult but flecked as a juvenile. Unlike the lion, however, the flecks
are not laid down as rosettes and the species is therefore coded flecked.
FEUD COAT PATTERNS
39 1
Lebtailurus serval. serval. The coat of this species is marked with flecks that can vary
gr'eatly in size and distinctness depending on the population (Weigel, 1961; Peters,
1982).
Caracal caracal, caracal. Another species with a uniformly coloured adult coat. The
juvenile coat is poorly known, though a few adult individuals have reddish brown
flecks on the legs and belly. However, we here consider the caracal coat pattern
uniform.
Fronailurus bengahis, leopard cat. A variably coloured cat for which the basic coat
pattern seems to be one of flecks that may run together to form bands.
Pronailurus viverrinus, fishing cat. The basic coat pattern of this cat is similar to that
off! bengahis, except that eumelanin dominates instead of phaeomelanin as in the
latter species. Coded as flecked.
Fronailurn planiceps, flat-headed cat. Another cat with a uniform adult coat pattern.
We have found no record of the juvenile coat pattern, but a few adults tend to have
the insides of the legs and the belly white flecked with brown. However, we have
coded this species as uniform.
Pronailurns rubiginosus, rusty-spotted cat. The coat of this cat is very much like that
of the leopard cat, except that it has a different colour phase. The flecks are rusty
brown on a brownish grey background instead of black on a yellowish background.
P r ~ e l i stemminckii, Asian golden cat. As noted above, the adplt coat pattern of this
species is extremely variable, being most uniform or flecked or with blotches. Other
variants can exist. We have here considered the species to be polymorphic (equivocal
in the analyses).
profelis aurata, African golden cat. The comments noted for F h m i n c k i i also apply
to this species, although the flecking is more apparent here.
profelis badia, bay cat. One of the least known of all species, never until recently
having been observed alive (Sunquist et al., 1994). The known skins are variable,
but most are uniformly chestnut coloured. Other specimens represent a grey colour
phase but are otherwise similar. It is coded as uniform herein.
Fe1i.s gbicu, African wild cat. The cats of the genus Felis are generally variable in
their coat patterns, but this species like the majority tends to have vertical stripes,
although flecked individuals are known. We have coded it as having vertical stripes.
Felis silvestris, European wild cat. This species tends generally to have its coat
patterned with vertical stripes.
Felis cajia. This species is not universally regarded as valid. It is included here because
of its uncertain phylogenetic status in the analysis of Salles (1992). Like the two
preceding forms the coat tends to have vertical stripes.
Felis bieti, Chinese desert cat. A very poorly known species, closely related to E
silvestris. Like E silvestris it has a coat patterned with vertical stripes, although these
are indistinct due to the pale fur.
Felis margarita, sand cat. A rare, desert dwelling cat with a pale coat with faint flecks
or stripes on the back and sides and banded legs and tail. Coded as vertical stripes.
392
L. WERDELIN AND L. OLSSON
Felis nignpes, black-footed cat. This small cat, unlike the majority of species in Felis,
has a coat patterned with distinct flecks that sometimes run together to form bands.
Felis chaus, jungle cat. Another uniformly coloured species. The juveniles have a coat
with clear vertical stripes that sometimes persist in the adult. Coded as vertical
stripes.
Otocolobus manul, Pallas’ cat. This species has a very long fur with generally indistinct
markings. However, when visible these tend to be in the form of vertical stripes.
Leopardus pardalis, ocelot. The ocelot has a coat pattern of black lines, flecks and
fields which tend to form blotches, although these are smaller than the blotches of
Jv. nebulosa and I! manorata and form a separate category in our coding.
Leopardus wiedii, margay. The coat of the margay is in every particular extremely
similar to that of the ocelot.
Leopardus t&$nus, oncilla. The oncilla’s coat resembles that of the ocelot and margay,
although there is a tendency to see rosettes in the patterns. We still consider this
species to have small blotches, however.
Leopardus colocolo, pampas cat. This species, which like the jaguarundi exists in a
reddish brown and a silver grey colour phase, has a coat with small blotches that
may in some pDpulations consist of flecks laid down as rosettes (Garcia-Perea, 1994).
It is here considered polymorphic.
Leopardus geofiyi, Geofioy’s cat. This species has a coat with a distinct pattern of
flecks.
Leopardus g u b a , kodkod. This poorly known form is another species with flecks that
sometimes run together to form bands.
Oreailumjacobitus, Andean mountain cat. This is probably the least known of all
cat species with the possible exception of I! badia. The available material indicates
that the coat, unlike that of other South American cats, is patterned with vertical
stripes.
CHARACTER EVOLUTION
In order to test Weigel’s (1961) hypothesis regarding the evolution of felid coat
patterns we used MacClade 3.0 (Maddison & Maddison, 1992) to map the coded
character states onto the phylogenies that have been described above. The procedure
is exemplified here using the phylogeny we derived from Salles’ (1992) data (Fig.
3).
From this figure we can calculate which character state transformations that have
occurred in felid phylogeny and their relative frequencies using all possible resolutions
FEUD COAT PATTERNS
393
TABLE
2. Average number of coat pattern transformations in the 466 trees obtained from analysis of
Salles (1992) data, averaged over all trees and all resolutions of ambiguous nodes, with polytomies
randomly resolved. Actual ranges are given in parentheses
~~
To
0
From 0
I
2
3
4
5
1
2
3
4
5
1.06 (0-2)
2.26 (2-3)
0.67 (0-1)
1.19 (0-2)
0.33 (0-1)
0.04 (0-1)
0
0
1.60 (0-2)
0
0
0.40 (0-1)
0.32 (0-1)
0.004 (0-1)
3.57 (2-4)
0
0
0.47 (0-2)
1
0.05 (0-2)
0.20 (0-1)
0.02 (0-1)
0.19 (0-1)
0.19 (0-1)
0
0
0
0
0.10 (0-1)
Figure 5. Coat pattern transformation seen in felid evolution as obtained from the phylogeny in Fig.
4. Number are rounded off to the nearest whole number of changes. The exact numbers are given in
Table 2.
of ambiguous areas in the phylogeny. The results are presented in Table 2 and
Figure 5 in terms of the average number of each possible character state change
per tree over all 466 equally parsimonious trees. In Table 2 the range in the number
of changes is also reported for each type of change. It can be seen that while some
character state changes are quite common, occurring several times per tree, others
are uncommon, while still others are entirely excluded by the topology of the trees.
The number of changes per tree ranges between 12 and 14 over all 466 trees.
In order to ascertain whether the set of character state changes found for the 466
trees differs from a random set we generated 466 random trees and mapped the
characters onto this set of trees. The character state changes found in this set of
L. WERDELIN AND L. OLSSON
394
TABLE
3. Average number of coat pattern transformations in 466 random trees, averaged over
all
trees and all resolutions of ambiguous nodes
To
0
From 0
I
0.31
1.79
2
0.08
3
4
5
0.17
0.31
1
2
2.28
4.45
0.34
0.84
0.06
0.12
0.18
0.12
0.22
0.32
3
4
5
1.23
1.71
0.15
0.66
0.05
2.31
0.18
0.84
0.05
0.1I
0.09
0.49
0.07
0.09
0.16
-
-oReal trees
Random trees
5000
Figure 6. Comparison between real and random trees in the number of each possible state change
present. Vertical bars represent one standard deviation.
trees are given in Table 3. In this case, although some character state changes are
more frequent than others, all can be seen to occur at least once among the 466
trees. In addition, the number of changes per tree is 14-22, which is substantially
more than in the 466 actual trees.
A comparison between the character state changes in the actual trees and those
in the random trees can be seen in Figure 6. The figure shows that not only is the
pattern of character state changes different between the two sets of trees but the
standard deviations of the number of character state changes over all trees are much
lower in the actual trees than in the random ones. This indicates that the actual
trees are significantly different from the random ones and that the reconstructions
of character states obtained from the actual trees have not been obtained by chance
alone. The differences in the number of each type of change between actual and
random trees were tested for equality using the Mann-Whitney U-test (as the variates
FELID COAT PATTERNS
395
TABLE
4. Results of Mann-Whitney U-test comparing numbers of each type of change between actual and random
trees. * =significant at 5%-level,** =significant at 1%-level,
*** =significant at 0.1%-level,NS =not significant
Change
(corrected for ties)
Significance
0->I
0->2
0->3
0->4
0->5
22.105
21.991
0.476
3.259
24.041
***
***
12-0
10.036
17.295
19.478
14.502
15.886
1 1.044
16.071
14.769
23.681
24.889
0.737
17.857
2.855
9.307
27.818
2.546
13.694
18.022
9.948
10.608
17.534
15.878
19.702
24.903
14.238
***
***
***
***
***
***
***
***
***
***
I->2
1->3
1->4
1->5
2->o
2-> I
2->3
2->4
2->5
3->O
3-> 1
3->2
3->4
3->5
4->O
4-> I
4->2
4->3
435
5->O
5 31
5->2
5->3
5->4
NS
***
***
NS
***
***
***
***
**
***
***
***
***
***
***
***
***
***
are non-normally distributed). The results are shown in Table 4,where it can be
seen that nearly all pairs are significantly different. This shows that our results are
not simply the result of assigning taxa to a random phylogeny.
The other two phylogenies are analysed in the same way in Figure 7A and 7B
and Tables 5 and 6. It can be seen that, although the actual numbers are different,
the pattern of character state changes in these figures is the same as that in Figure
5 , depicting Salles’ (1992) phylogeny. The two exceptions are the presence of changes
from vertical stripes to uniform and vice versa allowed by Herrington’s (1986)
phylogeny. It is evident, however, that these analyses support that reported above
in that only a small subset of all possible state changes are actually likely to have
occurred in felid phylogeny, many fewer than would be expected from a random
phylogeny of the Felidae (cf. Tables 2, 3, 5 and 6).
In summary it can be said that despite the many differences between the
phylogenies used in this study the results obtained from them are very similar,
indicating a significant degree of robustness in the analysis, the uncertainty regarding
felid interrelationships notwithstanding. In all cases flecks are reconstructed as the
primitive character state within the Felidae and the pattern of character transformations is very similar. There are 30 possible character state changes in this data
396
L. WERDELIN AND L. OLSSON
Figure 7. Coat pattern transformations seen in felid evolution as obtained from the phylogenies in Fig.
3A, B. Numbers are rounded off to the nearest whole number of changes. The exact numbers are
given in Tables 4 and 5, respectively.
set, 22 of which have some probability of occurrence, but only 12 of which are
present in a significant number of the possible trees. Most significantly, the character
state transformations predicted by Weigel’s (196 1) hypothesis of coat pattern evolution, which mainly involve a breakup of large patterns to form smaller ones, are
FEUD COAT PATTERNS
397
TABLE
5. Average number of coat pattern transformations in Herrington’s(1986) phylogeny, averaged
over all 36 resolutions of ambiguous nodes
To
0
From 0
I
2
3
4
5
0
1 .oo
0
0
0
I
2
3
4
5
0.67
2.67
I .oo
0.67
0.33
0
2.00
0
0
0
3.67
0
0.33
0
0
0.33
0
0
0
0
0.33
0
0
0
0
TABLE
6. Average number of coat pattern transformations found in 1000 random resolutions of the
phylogeny of Collier and O’Brien’s (1985) phylogeny, avertged over all resolutions of ambiguous nodes
To
0
From 0
I
2
3
4
5
1
2
3
4
5
0.84
1.09
0.9 1
1 .89
0.10
0.01
1 .oo
0
4.00
0
0
0
1
0
0
0
0.05
0.1 1
0
0
0.01
0
0
0
0
0
0
0
0
0
contradicted by the phylogenetic history of the group. We thus consider this
hypothesis as falsified by the data.
An alternative hypothesis suggests itself from Figures 5-7. In this hypothesis flecks
is the primitive state for felids and the one from which nearly all other patterns
spring. Only a few state changes bypass the flecked state. A process of coalescence
rather than breakup is thus evident. Significantly, there is no indication of any
ordered transformation series among the character states. There is thus no indication
that some states are intermediate betwken others, nor does it appear that a change
from flecks to rosettes is markedly easier (‘cheaper’ in the sense of parsimony) than
a change from flecks to uniform coat colour.
DISCUSSION
Recently, Ortolani & Car0 (1996)studied the adaptive significance of coat colour
patterns in carnivores, including felids, using methods in part similar to ours. It is
instructive to consider the similarities and differences between our approaches as
they relate to the set goals in the respective papers. Our goal here has specifically
been to reconstruct the changes in character state that are hypothesised to have
occurred in felid evolution and to use these to test a specific hypothesis available
for this evolution. The goal of Ortolani & Car0 (1996) was to reconstruct patterns
of correlation between coat colour patterns and specific environmental variables,
again to test previously available hypotheses.
This difference in aim has led to a general difference in coding practice. Herein
we have wished to avoid consideration of ontogenetic colour change within species
’
398
L. WERDELIN AND L. OLSSON
and thus we have coded lions as having rosettes despite these being more or less
lost in ontogeny. Ortolani & Caro (1996), on the other hand, have coded lions as
uniform since their interest has mainly been focused on the adaptive value of the
adult coat in its natural environment. Both of these approaches are correct in their
given contexts.
Ortolani & Caro (1996) have subdivided the carnivore body into a number of
areas, to test specific hypotheses of coat colour in those areas. We, on the other
hand, being interested to a large extent in hypotheses of mechanism such as that of
Murray (1 988), have used what could be considered ‘overall pattern’, which corresponds roughly to areas 1-5 of Ortolani & Car0 (1996, fig. 4.1). On the other
hand, we have used more character states (six) in our analysis than Ortolani &
Caro, who used only four. Again, this corresponds closely to our respective aims.
For us the distinction between flecks and rosettes is important, while for Ortolani
& Car0 (1996) it is not, as no adaptive hypothesis has to our knowledge been
formulated to explain this difference.
Finally, however, it should be noted that despite the differences in aim, approach
and data, Ortolani & Caro (1996) arrive at the same conclusion as we do herein,
that flecks (spots in their terminology) are unequivocally primitive in felids.
A few authors have considered particular aspects of coat pattern evolution in
felids. Kingdon (1977) suggested on the basis of variation within R pardus that the
coat patterns of this species were a result of small flecks fusing to form larger spots
and rosettes. On the basis of the data presented here this appears to be exactly
correct as part of the general pattern of felid coat pattern evolution. Peters (1982)
discussed the formation of uniform coat patterns in certain felids. Since there are
only a few species that can be said to have a uniform coat pattern in the sense
adopted here, Peters’ discussion lies somewhat outside the scope of the present work.
However, if one considers coat patterns in felids to have evolved from small flecks
to larger spots and fields, Peters’ hypothesis that uniform coats in, e.g. R temminckii
are due to a coalescing of these fields is in line with our data.
Turing-type models of pattern formation predict that the size of the animal at
the time when pigment pattern formation<isinitiated is an important parameter
determining the qualitative type of pattern that forms. If we assume a correlation
between adult size and the size at which the pattern is formed, this prediction can
be tested using the data presented here. With increasing size cats should have
uniform patterns, blotches, small blotches, rosettes, flecks, and uniform patterns
(again). Vertical stripes f d outside this characterization. In Table 1 we show the
size ranges of felids exhibiting the different patterns in felids. The predictions are
falsified, since cats of all sizes have flecks, cats with blotches are not smaller than
cats with small blotches, and the uniform species are neither the largest nor the
smallest cat species. It is also evident from Table 1 how different in size one of the
species with vertical stripes (R tgri~)is from the other striped species. This, taken
together with the phylogenetic position of the tiger and the fact that its stripes are
the only ones that show no sign of being coalesced spots, suggests that they are not
homologous to vertical stripp in other felids in either the developmental or the
phylogenetic sense of the word. In fact, it may be argued that the tiger simply has
rosettes that are greatly vertically extended, giving them a secondary appearance of
stripes.
As mentioned earlier, transformation series are seldom predicted in papers
modelling felid coat patterns. Generally speaking, the models may predict certain
FEUD COAT PATTERNS
399
selected transformations,but they fail summarily in predicting the actual interspecific
transformation series observed in the phylogeny. Young (1 984), however, shows that
a transition from flecks to stripes or a mottled pattern occurs in simulations based
on his model when the inhibition is decreased. Such a coalescence of flecks to form
stripes is in line with our results and also explains how the seemingly drastic change
in pattern between the cheetah and the king cheetah can depend on a simple shift
in a pattern formation parameter (in accord with the simple genetic change underlying
the king cheetah phenotype).
We hope that our work can stimulate modellers to reconsider the role of scale
and geometry for pigment pattern formation in felids and look at their models and
simulations with transformation series in mind. Information about how easy or
difficult it is for a pattern to change in a certain direction can shed light on the
important question of the role of developmental factors in macroevolution. Our
results show that not all possible character state changes take place. Is one reason
for this that some changes in the developmental mechanisms that create the coat
patterns are less likely than other changes?
CONCLUSIONS
In this paper we have demonstrated using phylogenetic techniques that Weigel’s
(1 96 1) hypothesis regarding the evolution of felid coat patterns is contrary to what
we know about the evolutionary history of the group. We instead propose a new
theory in which most transformations of coat pattern originate from the flecked
pattern, which we consider to be primitive for the Felidae as a whole. It is
important to note that we have used several currently competing theories of
felid interrelationships in developing this theory and that despite their mutual
inconsistencies they all support very nearly the same pattern of transformations. In
this instance the uncertainty regarding the phylogeny of the group has actually
rendered the hypothesis stronger, as it holds true under a relatively wide range of
conditions.
We also conclude that current developmental models of coat pattern formation
do not take sufficient account of phylogeny. We believe that the modelling approach
would benefit greatly from a consideration of those transformations that can be
demonstrated on phylogenetic grounds to have occurred within a group, since these,
rather than all possible transformations between character states, merit special
consideration. In this way phylogenies, along with careful study of developmental
anomalies, can help to shed light on developmental pathways and limitations.
ACKNOWLEDGEMENTS
This paper originated out of discussions at a course in systematics in part organised
by LW and financed by the Nordic Academy for Advanced Study, whose sponsorship
of this course is gratefully acknowledged. We are grateful to Gustav Peters, Victor
Albert and three reviewers for valuable comments on the manuscript. The research
of LW is financed by the Swedish Natural Science Research Council.
400
L. WERDELIN AND L. OLSSON
REFERENCES
Collier GE, O’Brien SJ. 1985. A molecular phylogeny of the Felidae: immunological distance.
Evolution 39: 473-487.
Eaton RL. 1976. A possible case of mimicry in larger mammals. Evolution 30 853-856.
Ewer RF. 1973. The Camims. London: Weidenfeld and Nicolson.
Garcia-Perea R. 1994. The pampas cat group (genus Lymhailuw Severtzov, 1858) (Carnivora:
Felidae), a systematic and biogeographic review. American Museum Novitutes 3096: 1-35.
Godfrey D, LythgoeJN, Rumball DA. 1987. Zebra stripes and tiger stripes: thc spatial frequency
distribution of the pattern compared to that of the background is significant in display and crypsis.
BiolagialJournal ofthe Linnean So&& 32: 427-433.
Hemmer H.1967. Untersuchungen zur Stammesgeschichteder Pantherkatzen (Pantheriiiac).Teil I.
Viniffentlichungen der ~oologi.schmStaatssammlung M2nchen 11: 1-121.
Herrington SJ. 1986. Phylogenetic relationships of the wild cats of the world. Unpublished Ph. D.
dissertation, University of Kansas, Lawrence.
Kingdon J. 1977. East Ajhtan Mammals. An A t h ofEvolution in Ajkca. Vol. ZZU. Carnivores. London:
Academic Press.
Kitchener A. 1991. lh Natural Histoy of Whi Cats. London: Christopher Helm.
Maddison WP,Maddison DR. 1992.MacCMe: anabsk ofphylogeny and character evolution. Sunderland,
Mass.: Sinauer.
Mohr E. 1967. Zur Fellzeichnung von Puma-Welpen, Puma concolor (Link, 177 1). Saugetierkundluhe
Mitteilungen 15: 170-1 72.
MumayJD. 1981a.On pattern formation mechanisms for lepidopteran wing patterns and mammalian
coat markings. Ptrilosophical Trransacliofir ofthe Royal So&&, London B 295: 473-496.
MurrayJD. 1981b. A pre-pattern formation mechanism for animal coat markings.Journu1 of Theoretical
BWlao 88: 161-199.
Murray JD.1988. How the leopard gets its spots. Scient3fic A d a n 311988: 62-69.
Murray JD. 1993. Mathematical Bwlog (2nd ed.). Heidelberg: Springer-Verlag.
Ortolani A, Car0 TM.1996.The adaptive significance of colour patterns in carnivores: phylogenetic
tests of classic hypotheses. In: Gittleman JL,ed. Carnivore BehavMr, fiology, and Evolution, volume 2.
Ithaca, Cornell University Press: 132-188.
Peters G. 1982.Zur Fellfarbe und -2eichnungeiniger Feliden (Mammalia, Carnivora).Bonner zoologische
Beitr@e 33: 19-3 1.
Pocock RI. 1910. The significance of the pattern of the cubs of lions (Felis leo) and of pumas (Felir
concolor). Annals and Magazine ofNatural Hisky (7)20: 436-445.
Salles L. 1992.Felid phylogenetics: extant taxa and skull morphology. American Museum Nouitutes 3047:
1-67.
Seidensticker J, ed. 1991. Great Cats. London: Merehurst.
Sunquist My Leh C,Sunquist F, Hills DM, Rajaratnam R. 1994. New record of the Bornean
bay cat. Cut New 20: 13-1 5.
Swofford DL. 1990. PAUP: phylagenetic anabsis .ring parsimoy. Urbana, Ill.: Illinois Natural History
Survey.
Turing AM. 1952. The chemical basis for morphogenesis. Philosophical fiansactions of& Royal So&&,
B 237: 37-72.
Van Aarde RJ, Van Dyk A. 1986. Inheritance of the king coat colour pattern in cheetahs Acinonyx
jubatus. Journal of zoolog,London 209: 573-578.
Weigel I. 1961. Das Fellmuster der wildlebenden Katzenarten und der Hauskatze in vergleichender
und stammesgeschichtlicher Hinsicht. Sliugetkhndliche Mittdungen 9: 1-1 20.
Young DA. 1984.A local activator-inhibitor model of vertebrate skin patterns. Mathematical BiosCimces
72: 51-58.