zoological Journal o f t h e Linnean Socieg (1987), 9I: 325-341. With 5 figures
The cybotoid anoles and Chamaelinorops
lizards (Reptilia:Iguanidae): evidence
of mosaic evolution
SUSAN M. CASE
Department of Biolou, Salem State College, Salem, M A 01970, U.S.A.
AND
ERNEST E. WILLIAMS
Museum of Comparative <oology, Harvard University,
Cambridge, M A 02138, U.S.A.
Received August 1986, accepted f o r publication December 1986
Recent immunological comparisons involving the Hispaniolan Chamaelinorops and Anolis suggested
that Chamaelinorops might be much more closely related to Hispaniolan species of Anolis than
previously thought. Electrophoretic comparisons among the relevant taxa, coupled with a review of
both the morphological and immunological data, suggest mosaic evolution may be responsible for
the nonconcordance between some of the data sets. An example of significant morphological change
with little electrophoretic differentiation was found in the A. cybotes-A. shrevei comparison while the
converse was found in the A. cybotes-A. marcanoi comparison. Many of the character states that have
been interpreted as implying close genealogical relationship between Chamaelinorops and other
Hispaniolan anoles are known to be primitive and may be evolving slowly in these lineages.
KEY WORDS:--Analis
Chamaelinorops - mosaic evolution
morphology - immunology - Hispaniola.
~
-
nonconcordance
-
electrophoresis
-
CONTENTS
Introduction . . . . . . . . . . . . . . . . . . .
Material and methods . . . . . . . . . . . . . . . . .
Morphology . . . . . . . . . . . . . . . . . .
Electrophoresis . . . . . . . . . . . . . . . . .
Results . . . . . . . . . . . . . . . . . . . .
Morphological and biochemical comparisons within the Anolis cybotes superspecies .
Biochemical comparisons between Anofis cybotes and noncybotoid Anolis . . . .
Morphological and biochemical comparisons between Anolis cybotes
and Chamaelinorops barbouri.
. . . . . . . . . . . . .
Discussion.
. . . . . . . . . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . . . . . . .
References. . . . . . . . . . . . . . . . . . . .
Appendix I
. . . . . . . . . . . . . . . . . . .
Appendix 2 . . . . . . . . . . . . . . . . . . .
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0 1987 T h e Linnean Society of London
326
S. M. CASE AND E. E. WILLIAMS
IN‘IRODIJCTION
Recently, the classification of Anolis has been cited as an example of
discordance between morphological evidence and karyotypic, electrophoretic
and immunological evidence of relationships (Gorman, Buth & Wyles, 1980;
Wyles & Gorman, 1980a; Shochat & Dessauer, 1981). T h e relationships
suggested by the immunological comparisons appear to conflict with the
‘established’ classification (Etheridge, 1960; Williams, 1976) based primarily on
osteology. ‘I’his led Wyles & Gorman (1980a) and also Gorman, Lieb &
Harwood ( 1984) to suggest that similar karyotypes and low immunological
distances may be more important indicators of relationships within Anolis at
higher taxonomic levels than are osteological criteria.
Wyles & Gorman (1980a) based their initial conclusions on a series of thirty
immunological comparisons. Antisera made against the albumin of the
Hispaniolan species Anolis cybotes Cope was reacted with the albumins of Anolis
species from Hispaniola, Puerto Rico, Cuba, Jamaica, the Bahamas, Mona, St.
Croix, Dominica, Barbados, Mexico, Malpelo Island in the eastern Pacific, as
well as the Hispaniolan genus Charnaelinorops Schmidt. This represented a broad
spectrum in terms of both conventional geography and geographic distribution.
When ranked in order of immunological distance (ID), the first seven species
closest to A . cybotes were all Hispaniolan (ID in parentheses): A . marcanoi
Williams (5); A . whitemani Williams (5); A . etheridgei Williams (25);
Chamaelinorups barbouri Schmidt (25); A. christuphei Williams (28); A. barahonae
Williams (28); and A . chlorocyanus Dumeril & Bibron (30).
Since the first two species were considered by Williams (1976) to belong to
the same superspecies that includes A. cybotes, the results with these species
occasioned no surprise. The remaining five, howevcr, are a miscellaneous lot.
The species referred to Anolis belong to two different subsections, three series
and three species groups according to Williams’ 1976 classification. Still more
surprising is the immunological placement of Chamaelinorops. Recognized as a
valid genus since its initial description in 1919, it is one of the two taxa outside
the cybotes superspecies that are closest to A . cyboles. The interpretation offered
by Wyles & Gorman (1980a) is that A . cybotes and the seven species
immunologically most similar to it represent a ma-jor radiation on Hispaniola.
It is not our purpose to question the Wyles & Gorman (1980a)
immunological data. We accept the immunological data, and we can confirm
and expand the evidence of nonconcordance with morphology to include
electrophoretic comparisons. However, we do question both the conclusions that
Wyles & Gorman (1980a) have drawn from their data and the expectation of
concordance itself.
With the aid of electrophoretic data we test the Wyles & Gorman (1980a)
hypothesis of presumed close genealogical affinity between the A . cybotes
superspecies and other Hispaniolan anoline taxa, especially Chamaelinorops.
Examined are eight populations belonging to seven taxa: two populations of
A . cybotes, two other members of the cybotes superspecies, two other Hispaniolan
species and one Puerto Rican species of Anolis (also included in the study of
Wyles & Gorman, 19804, and Chamaelinorops barbouri. T h e electrophoretic data,
summarized as Nei genetic distances, will be compared with Wyles & Gorman’s
( 1980a) immunological distances and both will be compared with morphology.
We offer an alternative interpretation of the evidence. Morphology and
MOSAIC EVOLUTION IN ANOLINE LIZARDS
327
albumins have evolved at different rates; the albumins of many Hispaniolan
anole species are relatively similar because they have been evolving slowly. This
is another expected example of the phenomenon of mosaic evolution.
MATERIAL AND METHODS
Morphology
The external characters of the cybotoid assemblage have long been known
(Cochran, 1941; Williams, 1963, 1975; Schwartz, 1979). The osteology is also
well known (Etheridge, 1960). Species characteristics were taken from the
literature cited above. Since all cybotoid taxa are available in series and as dry
skeletons in the collections of the Museum of Comparative Zoology, characters
for all taxa have been checked to reconfirm them.
Chamaelinorops barbouri has, until recently, been relatively rare and poorly
reported. The externals have been reported by Schwartz & Inchaustegui (1980)
as well as by Schmidt (1919, 192 l a ) and Thomas (1966). More recently there
have been careful studies of the vertebral column by Forsgaard (1983) and of
the toe pads by Peterson (1983). Cranial osteology and the shoulder girdle have
been studied by Etheridge ( 1960, and unpublished). The inscriptional ribs have
been reported by Etheridge ( 1965). For C ~ a r n ~ e ~ i n o rbarbouri,
o~s
cleared and
stained specimens, including both hatchlings and adults, dry skeletons and
preserved specimens are available. The latter material is the result of large
recent collections of C. barbouri made in the Sierra de Baoruco, Dominican
Republic after the review of Schwartz & Inchaustegui (1980). This is also the
source of the specimens used by Wyles & Gorman (1980a) for immunology and
by us for electrophoresis. The new material permits re-examination of all prior
reports.
The only morphological data never previously examined is that provided by
scanning electron microscopy of the skin. For scanning electron microscopy,
entire hatchlings of Chamaelinorops and of the Anolis species examined were small
enough to be placed on a suitable stub. After critical point drying, they were
coated with gold and palladium. Detached scales were similarly treated.
Polaroid pictures were taken of critical views as seen on the screen of an AMR100 SEM instrument. Pictures bear dates and numbers as well as magnification.
Electrophoresis
Tissue from seven taxa represented by 138 animals were examined
electrophoretically on starch gels. Table 1 lists the taxa, localities, sample sizes
and sources of material. Most of the tissue extracts were prepared by the late
T . P. Webster in the mid-1970s and were stored a t -70°C until use in
1978-1979. Because he made whole animal extracts, no voucher specimens for
his samples are available. Vouchers for our samples of Chamaelinorops barbouri and
Anolis marcanoi, obtained in 1978 and 1980, respectively, are deposited in the
collections of the Museum of Comparative Zoology, Harvard University.
A total of 11-14 loci were anaiysed for each species. Methods of tissue
preparation and electrophoretic analysis follow Selander, Smith, Yang, Johnson
& Gentry (1971) and Ayala, Powell, Tracey, Mourao & Perez-Salaas (1972).
S. M. CASE AND E. E. WILLIAMS
328
Table 1. Taxa used in this study, including sample size (A'), locality and source
(TPW = T. P. Webster; C & W = Case & Williams)
N
'I'axon
Locality
Source
-
Anolis cybotes
36
A. cybotes
A . shrevei
19
26
1
A . marcanoi
A . elheridgei
A . christuphei
27
27
A . cuuieri
Chamaelinorops barbourt
1
1
Dominican Republic: La Vega Prov
Jarabacoa
Haiti: Dept. L'Ouest, Thomazeau
D.R.: La Vega Prov., Valle Nuevo
& Valle Verde
D.R.: Peravia Prov., Bani 1st ford
on El Recodo rd.
D.R.: La Vega Prov., La Palma
D.R.: La Vega Prov., La Palma
& El Rio ravine
Puerto Rico: El Verde
D.R.: Barahona Prov., Avi Acmar
TPW
TPW
TPW
C&W
TPW
TPW
v w
C&W
Table 2 summarizes the loci studied and the buffer systems used. If an enzyme
was encoded by two or more loci, loci were numbered in order of decreasing
mobility. Similarly, alleles at a single locus were listed in order of decreasing
mobility, the fastest being a, etc. Allele designations used here are taken from a
larger study of Hispaniolan anoles and are equivalent to the alleles listed there
(Williams & Case, unpublished). Nei's genetic distance (DN)
(Nei, 1971) was
calculated from allele frequencies for each species pair, using only those loci for
which information was available for both species. The heterogeneity of allele
frequencies among the cybotoid taxa was examined using the method of
Workman & Niswander (1970).
RESULTS
Morphological and biochemical comparisons within the Anolis cybotes superspecieJ
The marked differences in the levels of morphological differentiation among
cybotoid anole species are summarized in Table 3. The three cybotoid taxa
studied here display these differences well. Populations of Anolis cybotes are
Table 2. Summary of enzyme loci examined and buffers used'
~~~
Enzyme
Abbreviation
Isocitratc drhydrogrnase
Phosphoglucornutase
Aspartate aminotransferase
Malate dehydrogenase
Mannosephosphate isomerase
6-Phosphogluconate dehydrogenase
Glycerol-3-phosphate drhydrogenase
Lactate dehydrogenase
Glucophosphate isomerase
General protein
General proteins
.~
~
~~~~~~~~
IDH
PGM-1 and 2
AAT
MDH
MPI
6PGD
G-3-PDH
LDH-1 and 2
GPI
GP5
GP2 and 4
E.C. no.
E.C. 1.1.1.42
E.C.2.7.5.1
E.C.2.6.1.1.
E.C.1.1.1.37
E.C.5.3.1.8
E.C.1.1.1.44
E.C.1.1.1.8
E.C.l. 1.1.27
E.C.5.3.1.9
Buffer
1
2
3
4
4
4
4
5
5
5
6
~~~~~~
* I = t r i s ~maleir~EDTA; 2 = continuous phosphate citrate (pH 6.7); 3 = phosphate ( p H
6.7); 4 = tris-citrate (pH 8.0); 5 = Poulik; 6 = lithium hydroxide.
MOSAIC EVOLUTION I N ANOLINE LIZARDS
329
Table 3. Comparison of selected morphological traits in some members of the
Anolis cybotes species group. Sources of information are cited in the text
Ventrals
Mid-dorsals
Temporals
Body colour
Dewlap colour
cyhotes
Smooth,
cycloid
Equal to or
smaller than
flank scales
c.
2 rows
abruptly
enlarged
Brown to
reddish
Pale yellow with
greyish streaks
or greyish with
yellowish streaks
marcanoi
Smooth,
cycloid
Equal to
flank scales
Tending to
grade into
flank scales
Brown with or
without obscure
markings
Rose-red anteriorly,
orange posteriorly,
purplish a t centre
longitibiatis
Smooth,
narrow
Equal to
flank srales
Abruptly larger Greyish with
streaking or brown
than flank
with darker markings
scales
Orange to dull
yellow
Jttahmi
Smooth,
narrow
Equal to
flank scales
Abruptly larger Grey unpatterned
or greyish with
than flank
scales
hourglass markings
Deep orange
whilemani
Keeled,
narrow
Distinctly
larger than
flank scales
Grading into
flank scales
Pale tan with
or without grey
transverse markings
White
shrevei
Keeled,
narrow
Distinctly
larger than
flank scales
Grading into
flank scales
Brownish to
dark grey
Dirty white
amouri
Smooth, Distinctly
cycloid
larger than
flank scales
Tending to
grade into
flank scales
Brown, often with
bold rhombs on
flanks
Pinkish or yellowish
with greenish smudges
centrally
morphologically indistinguishable, and there is no evidence of distributional
discontinuity. A. marcanoi, primarily allopatric to A. cybotes, differs sharply from
A. cybotes only in dewlap or throat colour; the few scale differences are such that
in the absence of colour not all specimens can be correctly assigned. Anolis shrevei
Cochran is more distinct. I t is a montane species and, like A. marcanoi, primarily
allopatric to A. cybotes. Webster (personal communication) did find A. cybotes
and A. shrevei together in apparent sympatry, but he felt this was the result of
truck transport and not a natural phenomenon. Although the gaps between the
distributions of these two species are a kilometre or less, no areas of overlap have
been confirmed. Anolis shrevei differs markedly from A. cybotes in body size and
shape, dewlap colour and the size and keeling of the scales.
The electrophoretic comparisons reveal a completely different pattern of
differentiation. The allele frequencies for all taxa examined are presented in
Appendix 1; the Nei distances between them are given in Table 4. Examination
of these data reveal the following:
(1) Anolis marcanoi is very distinct from other cybotoids examined. The Nei
distances range from 0.68-0.74, with an average value of 0.70.
(2) The other cybotoid populations are almost indistinguishable from one
another. The A . cybotes population from the Dominican Republic is slightly
more similar to A. shrevei than to the conspecific Haitian population. Anolis
shrevei does have rare alleles unique to it, but so do both A. cybotes populations
S. M. CASE AND E. E. WILLIAMS
330
Table 4. Nei's genetic distance (D)among
several species of Anolis and Chamaelinorops
barbouri"
Species
cybD cybH
shr
mar'
eth
chr
cuv'
~
cyhD
cybH
shr
mar
rth
chr
CUV
--
0.05
0.04
0.05
0.74
0.68
0.68
1.11
1.12
1.13
1.30
0.91
0.84
0.96
1.53
0.48
~
1.04
1.07
1.01
1.06
0.59
095
Cbii
-__
1.17
1.19
1.13
1.10
0.98
1.07
1.12
*Abbreviations used: cybl) = A . rybotrs, Dominican
Republic; cybH = A. ryboles, Haiti; shr = A. shrevei; niar = A .
ma7ranoi; e t h = A . etheridgei; chr = h. ci'iristophei; cuv = A . cuuieri;
rba = Chamaelinorops barhouri.
'Nri distances based on I 2 loci; 'Nci distances based on 13
loci: "Nci distancrs based on I 1 loci.
examined. The samples of A . cybotes and A . shrevei did show significant
heterogeneity of allele frequencies at four polymorphic loci when tested using
the method of Workman & Niswander (1970).
Biochemical comparisons between Anolis cybotes and noncybotoid Anolis
Three other species of Anolis were examined electrophoretically. Two species,
A. etheridgei and A . christophei, are Hispaniolan and are listed among the species
immunologically similar to A. cybotes (see introduction). T h e third species,
A. cuuieri Merrem, is Puerto Rican and immunologically is more distant (the
immunological distance from A . cybotes is 34; Wyles & Gorman, 1980a).
'l'he electrophoretic Nei distances between A . cybotes and each of these three
species are given in Table 4. Of the three species Anolis christophei appears to be
the closest to A . cybotes (with = 0.88) but all are quite distant. Anolis etheridgei
from Hispaniola is as distant from A . cybotes as is the Puerto Rican species,
A . cuvieri.
Morphological and biochemical comparisons between Anolis cybotes and
Chamaelinorops barbouri
The characters of Chamaelinorops are displayed in Appendix 2 and are
contrasted with those of the cybotoid anoles. They are a confusing roster. The
differences are found in many systems and are a mixture of the primitive, the
uniquely derived and the equivocal. It may be useful to categorize some of the
listed characters of Chamaelinorops.
Primitive; The high number of inscriptional ribs (Etheridge, 1965) is a more
primitive state than that found in A . cybotes. T h e karyotype (Gorman, 1973;
Paull, Williams & Hall, 1976) is as primitive as that of A . cybotes. (The
karyotype of Chamaelinorops has not yet been figured but a description is in
preparation (J. Blake, MS.) It already has been reported as 12
MOSAIC EVOLU'IION IN ANOLINE LIZARDS
+
33 1
macrochromosomes
24 microchromosomes in Paul1 et at. (1976, pp. 7 and
15).) The two types of skin sense organs seen i n the scanning electron
micrographs of Figure 1A and B a smaller sense organ with a single tall hair
and a larger hairless but evenly spinulate ('pillow') organ-are identical in the
two taxa. They are also seen in all other anoles examined (Chamaeleolis Cocteau,
I
100 p
I
Figure 1 . Sranning electron micrographs of head scales of Anolis cybotes (A) and Chamaelinorops
harhourz ( B ) . Two types of sense organs are visible in both the sense organ with a single tall hair
and the spinulate 'pillow' orpin. 'l'he difference brtween the two species in the background surface
texture is apparent.
S. M. CASE AND E. E. WILLIAMS
332
Phenacosaurus Barbour and approximately 100 species of Anolis; Williams,
unpublished) and so would be considered primitive for anoles.
Uniquely derived: The interzygapophysial wings (Forsgaard, 1983) and their
external counterparts, the projecting margins of a dorsal zone of enlarged scales
(Schmidt, 1921b) are found in no other anoline lizard. Figure 2 compares a
thoracic vertebra of Chamaelinorops with one of A . cybotes.
Equivocal: The laterally expanded caudal transverse processes, interpreted by
Etheridge (personal communication) as autapomorphic modifications of beta
anole caudal transverse processes, and hence presumably highly derived, have
been regarded by Williams (1977) as very primitive. Figure 3 compares a
middle caudal vertebra of Chamaelinorops with one of A . cybotes. Controversial as
these structures are, they cannot be reliable indicators of Chamaelinorops’
relationship. However, either interpretation would appear to make the genus
very remote from A . cybotes.
A
B
Figure 2. Comparison of mid-thoracic vertebrae in AnolL cybotes (A) and Chamaelinorops barbouri (B).
The views shown are, from top to bottom, lateral, dorsal, ventral, and anterior.
MOSAIC EVOLUTION IN ANOLINE LIZARDS
A
333
0
H
I rnm
Figure 3. Comparison of caudal vertebrae of Chamaelinorops barbouri (A) and Anolis cyboles (B). Both
are dorsal views: the anterior of the animal is at the top of the figure.
The interclavicle in Chamaelinorops is also very different from that of A . cybotes
(Figure 4). The interclavicle of Chamaelinorops is described as ‘T’, with the
interclavicular arms closely apposed to the clavicle. This contrasts with the
interclavicle of A . cybotes which is described as ‘arrow’ with the interclavicular
arms distinctly divergent from the clavicles. The difference is patent; the
interpretation is more difficult. The T condition is found in all beta anoles and
some alphas. T h e arrow condition is found in all other alphas, including
A . cybotes. The polarity of the transformation series is uncertain.
A
B
Figure 4. Comparison of the clavicles (open) and interclavicles (stippled) of Chamaelinorops barbouri
(A) and Anolzs gbotes (B).
334
S. M. CASE AND E. E. W I I M A M S
Similarly equivocal is the microstructure of the adhesive hairs on the toe in
Chamaelinorops. The tips of these ‘setae’ are described by Peterson (1983) as
quadrangular rather than triangular and their spacing and density is different
from that in all other examined anoles. Peterson’s (1983) figs 4B and 6F contrast
the condition in Anolis cuvieri (to which A . cybotes is similar) and Chamaelinorops,
respectively. Peterson’s ( 1983) summary is: “Functional interpretation can not
at this point resolve whether Chamaelinorops morphology represents a secondary
terrestrial adaptation of Anolis-like fine structure or an independent, perhaps
even a less successful ‘experiment’ in seta evolution.”
Differences in the skin microstructure are also difficult to interpret. Figure 1A
and B are scanning electron micrographs of head scale microstructure of Anolis
cybotes and Chamaelinorops, showing background surface texture and skin sense
organs (mechanoreceptors). The microstructural differences in spinule character
is very striking. Spinules are uniformly minute in A. cybotes, but vary markedly
between cells in Chamaelinorops. In comparison with other spinulate iguanids the
condition in A. cybotes appears to be more primitive than that in Chamaelinorops.
There are both some alpha and beta Anolis (e.g. A . aequatorialis, A . lionohs) that
approach the condition in Charnaelinorops but there is no close approximation
(Williams, in prep.). ‘lhe Chamaelinorops condition is best considered an
autapomorphy of the genus.
Appendix 2 cites only differences. It would seem that to be fair we should also
tabulate the morphological resemblances between cybotoids and C‘harnaelinorops.
Unfortunately it is impossible to prepare any list of the similarities of the two
taxa that goes much beyond a statement that both are anoles! T h e resemblances
of (,’hamaelinorops and cybotoids are either primitive or trivial. Both have anoline
dewlaps, toe pads that are basically similar in macrostructure, three sternal ribs,
postxiphisternal inscriptional ribs, a spinulate Oberhautchen, and two kinds of
skin mechanoreceptors found together only in anoles. All of these are, however,
defining characters for the entire anoline group. Both cybotoids and
Chamaelinorops have the 12V+24m karyotype, but this is shared not only with
many other anoles but many other lizards (Paul1 et al., 1976). There are, we
emphasize, no shared derived morphological characters that would indicate a
special genealogical relationship between Chamaetinorops and the cybotoids of
Hispaniola.
‘lhe electrophoretic comparisons summarized as Nei distances in ‘lable 4
indicate Chamaelinorops is distinct from all of the species examined. In general it
is as distinct from the Hispaniolan species of An0li.r ( D = 1 . 1 1) as it is from Anolis
cuvieri, the one Puerto Rican species examined (0= 1.12).
DISCUSSION
It has been noted time and again that the relationships between species
inferred from morphology are usually also recognized by biochemical
comparisons (e.g. Thorpe, 1982). However, now there are known a number of
examples from a variety of taxa in which such concordance has not been found
(see summary in Fuller, Lee & Maxson, 1984). Given that different characters
evolve at different rates, perhaps we should be surprised that there are not more
disagreements between data sets.
Within the anoline radiation there are several examples in which the
MOSAIC EVOLUTION IN ANOLINE LIZARDS
335
relationships inferred from morphology are different from those inferred from
biochemical comparisons. These apparent discrepancies led Wyles & Gorman
(1980a) and Gorman et al. (1984) to suggest that anole classification must be
totally revised at the higher levels, a proposition that appears to reject all of the
evidence from morphological comparisons. We will focus on two of these
examples of discordance and then discuss some of the broader implications.
The Anolis cybotes superspecies: T h e cybotoid anoles comprise eight taxa, all
Hispaniolan and all allo- or parapatric to one another. Williams ( 1976)
recognized seven members of a cybotes superspecies-A. cybotes, A . whitemani,
A . armouri Cochran, A . shrevei, A. longitibialis Noble, A . haetianus Garman, and
A . marcanoi. Schwartz (1979) recently described an eighth, A . strahmi. Only
A . cybotes is widespread; the other species have restricted ranges.
In the cybotoids examined to date it is clear that genetic distance is poorly
correlated with morphological difference or with species status as indicated by
other biological criteria. The discordance between the minor morphological and
major electrophoretic difference in the A . cybotes-A. marcanoi comparison was
first published by Webster in 1975. Gorman then (personal communication)
questioned the identity of Webster’s samples because of discrepancy between
Webster’s information and the close electrophoretic similarity expected in the
comparison of morphologically sibling species. Gorman and coworkers (later
published in Wyles & Gorman, 1980a) had made an immunological comparison
of the albumins of A . marcanoi and A. cybotes and had observed a n immunological
distance of 5. This suggested that the two species (or at least their albumins)
were very similar. Using different material and a partially overlapping set of loci
we confirm Webster’s findings of significant electrophoretic differentiation
between these two species.
While the A . cybotes-A. marcanoi comparison demonstrates little morphological
difference associated with major electrophoretic differentiation, the
A . cybotes A. shrevei comparison demonstrates the converse. I n this case there has
been considerable morphological differentiation but minimal electrophoretic
differentiation. Unfortunately, no immunological comparisons involving
A . shrevei have been made to date.
Anolis cybotes and Chamaelinorops: When Wyles & Gorman (1980a)
observed a low immunological distance between A. cybotes and Chamaelinorops,
they offered as one possible explanation the suggestion that Chamaelinorops might
have undergone rapid morphological evolution and be part of a n intraHispaniolan radiation of alpha anoles.
Chamaelinorops, recognized as a distinct genus since its description by Schmidt
in 1919, is represented by a single montane species. Williams (1961) divided
Hispaniola into ‘north’ and ‘south’ islands. Chamaelinorops is recorded on the
north island only from one specimen collected near Constanza in the Cordillera
Central. O n the south island it is known from the Massif de la Hotte and the
Massif de la Selle in Haiti and from the Sierra de Baoruco in the Dominican
Republic. The review by Schwartz & Inchaustegui (1980) confirm Thomas
(1966) in regarding all populations as conspecific.
How Chamaelinorops is related to other anolines is unclear. Few workers have
ventured to express an opinion about the placement of Chamaelinorops. Etheridge,
in a dendogram in Paul1 el al. (1976), placed Chamaelinorops near the base of the
336
S. M. CASE A N D E. E. WILLIAMS
H
I mm
Figure 5. A dorsal view of a caudal vertebra from a j-anole, Anolis sagrei (after Etheridge, 1967).
beta section of the anoles, based on the presence of caudal transverse processes.
Williams (1977), impressed by the strength of the caudal transverse processes in
Chamaelinorops (which he sees as quite unlike those of typical beta anoles;
compare Figure 3 with Figure 5 ) , and by their co-occurrence with a high
number of inscriptional ribs (which both he and Etheridge consider primitive)
and by a primitive karyotype, thought that the genus might have diverged
earlier, at the very base of the anoline radiation. While we cannot address the
question of the rate of morphological change in Chamaelinorops, the morphology
of Chamaelinorops does not, in our judgement, ally it with any specijic group of
Anolis. There certainly are no shared, derived characters that indicate
Chamaelinorops is especially closely allied to cybotoids or to any other
Hispaniolan species of Anolis.
Discordance between different types of data is being recognized as a pervasive
phenomenon (Fuller et al., 1984). In such a situation two questions arise: ( 1 )
how morphological difference should be interpreted; (2) how immunological
distance should be interpreted.
Morphological difference (patristic distance) may be an unreliable criterion of
phylogenetic affinity in many cases and so is often dismissed, as Wyles &
Gorman ( 1980a) have dismissed it. But morphological characters phylogenetically interpreted are the initial basis of all cladistic analysis. It might be
said in the present case that no phylogenetic conclusion can be reached with the
available evidence, but certainly it is inappropriate to assume unhesitatingly
that there is close affinity between two organisms when the morphological
differences are as great, and in as many systems, as those seen here. If Wyles &
Gorman are right, they have discovered one of the most remarkable instances of
rapid multistate morphological evolution known.
Immunological distance provides a linear measure of the difference between
two molecules, reflecting either the total number of amino acid differences or
the percentage of amino acid difference (Wilson, Carlson & White, 1977). They
cannot, however, indicate where in the molecule these changes have occurred.
When low immunological distances are observed, one must ask whether these
low values reflect shared synapomorphies (and close genealogical relationship)
or shared pleseiomorphies (and a slowly evolving molecule). T o answer this
question properly, comparisons with outside reference species are needed and
relative rate tests (Wilson et al., 1977) should be done.
MOSAIC EVOLUTION IN ANOLINE LIZARDS
337
It may well be that there has been one major Hispaniolan radiation, but, if
so, it may be an old one. Morphologically the Hispaniolan assemblage which
Wyles & Gorman (1980a) examined is a disparate assortment. Only two
characters that are not common to all alpha anoles group A . cybotes (cybotes
series), A . etheridgei and A . christophei (monticola series), A . barahonae (cuuieri series),
A . chlorocyanus (carolinensis series) and Chamaelinorops together (using Williams’,
1976, classification). These characters are the low immunological distance
measured from A . ybotes and the karyotype. The karyotype of all of these species
is 12 macro- and 24 microchromosomes, a karyotype that Gorman (1973) and
Paul1 et al. (1976) argued was primitive for all lizards. Karyotype in these
Hispaniolan species is then not a shared derived character but a shared
primitive one, a poor indicator of close relationship. May not the similarity of
albumins be also a shared primitive character?
Further comparisons and relative rate tests are needed before the low
immunological distances can be used to infer genealogical relationships. Less
direct evidence is available that has some bearing on this problem. Wyles &
Gorman (1980b) endeavoured to demonstrate a high correlation ( r = 0.83)
between Nei’s genetic distance and immunological distance in Anolis. Their
algorithm can be used to estimate expected values for either Nei’s distance or
immunological distance if the other is known.
I n Table 5, the observed immunological distance between the relevant
Hispaniolan species (Wyles & Gorman, 1980a) is compared to that predicted by
the Nei distance between them (data from this study). Although we did not use
the same loci as Wyles & Gorman (1980b) and so d o not expect a perfect
correspondence, we find the observed immunological distances to be consistently
lower than predicted (by a factor ranging from 1.7 to 6). This suggests that
albumin might be slowly evolving in one or several of these species. Wyles &
Gorman (1980a) considered this as another possible explanation for the case of
Chamaelinorops but apparently did not consider it in the case of any other species.
Different taxonomic features, including proteins, evolve a t different rates, the
well-known but frequently over-looked phenomenon of mosaic evolution. Wyles
& Gorman (19804 concluded their study with the observation that “Despite
Table 5. Comparison of
immunological distances
genetic distance. All Nei
reported here between
Comparison
(Antisera)-(Antigen)
A . cybotes-A. marcanoi
A . cybotes-A. etheridzei
A . cybotes-A. christophei
A . cyhotes-A. cuuieri
A . cybotes-Chamaelinorops
A . cuuieri-Chamaelinorops
observed and expected
predicted from Nei’s
distances (D)are those
cybD and other taxa
D
0.74
1.11
0.91
1.04
1.17
1.12
Immunological distance
__
Observed
Expected
5
25
27
34 ’
25
142
30
42
35
39
43
42
Observed immunological distances are taken from Wyles & Gorman
(1980a) except where noted. ‘Gorman el al. (1980) reported a
reciprocal distance of 51; the average of these two, 43, agrees well with
the predicted value. 2Gorman, personal communication.
S. M . CASE AND E, E. WILLIAMS
338
the seeming biogeographic coherence of the established classification of Anolis
the field is still open to analysis, and a major reinterpretation may be
necessary.” We agree that the field is still open to analysis arid point out that the
published morphological data pertinent to the field of Anolis classification have
not advanced much beyond Etheridge (1960). There are important
opportunities for advance in that area, for example in cranial osteology. When
there is nonconcordance, such as that documented here and by many others, it
is not reason enough for accepting one set of data or rejecting another. It is
instead an opportunity to re-evaluate old evidence and search for new
information that will clarify the processes responsible.
ACKNOWLEDGEMENTS
Wc thank D. Buth, R . Etheridge, G. Gorman, H. Lessios, G. Mayer,
J. Peterson, and J. Wyles for their comments on earlier drafts of this work.
E. Seling provided technical assistance with the scanning electron microscopy.
We also thank L. Meszoly for preparing the illustrations and photographs, and
C. McGeary for preparing the various drafts of the manuscript. This work was
supported by various National Science Foundation grants to E. E. Williams, by
Harvard University, and by the Bureau of Faculty Research, Salem Statc
College.
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APPENDIX I
Allele frequencies in several species of Anolis and Charnadinorops barbouri. 'l'he sample size is given in parentheses
following the species name. Abbreviations used: abs. = absent, nd = no data available.
A. cybotes, Dominican Republic (36): LDH-I, b(I.0); LDH-2, b(l.O); MDH, c(1.0); IDH, b(l.0); G-3-PL)H,
c(0.6), g(0.4); PGM-I, b(l.O); PGM-2, a(0.03), c(0.59), f(0.26), g(0.1), h(0.03); GPGD, c(0.07), d(0.85),
f(0.08); MPI, d(0.01), e(0.99); GPI, b(O.ll), e(0.71), h(0.18); AAT, c(1.0); GP2, "(1.0); GP4, a(I.0); GP5,
a(l.0).
A. cybotes, Haiti (19): LDH-1, b(l.O); LDH-2, b(1.0); MDH, c(i.0); IDH, h(l.O); G-3-PL)H, e(l.O); PGM-I,
h(l.O); PGM-2, b(0.06), c(0,26), f(0.68); GGPL), c(0.55), d(0.37), f(O.08); MPI, e(l.O); GPI, a(0.03), b(0.26),
c(0.61), f(0.03), h(0.08); AAT, c(1.0); GP2, a(l.O); G1'4, "(1.0); GP5, a ( l . 0 ) .
A . shreuei ( 2 6 ) : LDH-1, b( 1.0); LDH-2, h(0.98), ~ ( 0 . 0 2 ) MDH,
;
b(0.02), ~ ( 0 . 9 8 ) IDH,
;
b ( 1.0); G-3-PDH,
c(0.98), g(O.02); PGM-I, a(0.04), b(0.96); PGM-2, c(0.63), f(0.02), g(0.35); 6PGD c(0.08), d(0.52), f(0.4);
a ( 1.0); GP4, a(l.O); GP5, a(l.O).
MPI, b(0.04), e(0.96); GPI, b(0.54), c(0.44), h(0.02); AAT, ~ ( 1 . 0 )GP2,
;
A . rnarcanoi ( 1 ) : LDH-I, b(l.O); LDH-2, a(l.O); MDH, c ( l . 0 ) ; IDH, ~ ( 1 . 0 )G-3-PDH,
;
e(l.O); PGM-I, h(1.0);
PGM-2, abs.; GPGD, e(l.0); MPI, e(0.5), f(0.5); GPI, c(I.0); AA'I', "(1.0); GP2, nd; GP4, a ( l . 0 ) ; GP5, nd.
A . etheridgci (27): LDH-I, b(1.0); LDH-2, e ( 1.0); MDH, ~(1.0); IDH, c(1.0); G-3-I'DH, b(l.0); PGM-I,
c ( 1.0); PGM-2, f(0.09), h(0.89),j(0.02);GPGD, f(0.04), g(0.96);MPI, e(0.13), g(0.87); GPI, d(0.89),h(O.l I ) ;
A A I , b(l.O);GP2, "(1.0); GP4, b(0.98), ~ ( 0 . 0 2 )GP5,
;
a(l.0).
A . chrzstophei (27): LDH-1, b(1.0); LDH-2, e(l.O); MDH, d(l.O); IDH, c(1.0); G-3-PDH, b(l.O); PGM-1,
c(0.87), d(0.13); PGM-2, f(0.98), h(0.02); GPGD, g(0.17), i(0.8), j(0.03); MPI, a(0.15), e(0.85); GPI, d(l.O);
AA'I', ~ ( 1 . 0 )GP2,
;
a ( l . O ) ; GP4, d(l.O); GP5, a ( l . 0 ) .
A . muieri ( I ) : LDH-I, b(l.O); LDH-2, d(l.O); MDH, c(l.0); IDH, ~ ( 1 . 0 ) ;G-3-PDH, b(l.O); PGM-I, c(1.0);
1'GM-2, d(l.0); 6PGD, 111.0); MPI, g(l.O); GPI, h(l.O); AAI', e(I.O); GP2, nd; GP4, a(I.0); GP5, a(I.O).
Charnaelinorop.r barbonri (I):LDH-1, b(l.O); LDH-2, b(l.O); MDH, ~ ( 1 . 0 ) IDH,
;
c(1.0); G-3-PDH, d(l.O);
PGM-I, d(l.O); PGM-2, e(l.O); GPGD, f(0.5), i(0.5); MPI, f ( l . O ) ; GPI, d(l.O); AAT, d(l.O); GP2, nd; GP4,
nd; GP5, nd.
340
S. M. CASE AND E. E. WILLIAMS
APPENDIX 2
Characters of Chamaelinorops compared with those of the cybotoid anoles. Conditions unique (autapomorphic)
for Chamaelinorops are in italics. Sources of information are cited in the text or are based on: I-Peterson,
unpublished; 2 W. P. Hall, personal communication; 3-personal observation.
__
MACROSTRUCTURES
Dewlap
Toepads
SCALES
Nasal
Canthals
Dorsals
Flank scales
Ventrals
Postmentals
Chamaelinorops
In both sexes, small; smaller in
female
Narrow, on phalanges i and ii
A circumnasal, unmodified,
separated from rostral by 2 or more
scales
3
Highly differentiated zone of larger
and smaller imbricate keeled scales,
project laterally in distinct shelf aboue
smaller Jank scales
Size variable, smooth, juxtaposed or
subimbricate, with larger keeled
imbricate scales
Distinct from flank scales, countable,
with huge keels
2 large multicarinate postmentals
between infralabials, sometimes in
contact; never more than 2 medial
smaller scales, sometimes with smaller
lateral scales separating postmentals from
infralabials
SKIN MICROSTRUCTURE
Skin surface texture
Spinulate; great intercellular
variation in spinule height and
diameter
Quadrangular
Toe pad setae
Setal spacing different from all othei
anoles
SKELETON
Rugose surface with adherent skin
Skull
post frontal
Mandible
labial surface
Absent
splenial
coronoid
Dorsal vertebrae
Caudal vertebrae
Absent
Labial process short
Unique broad interugapophysial plates
Strong laterally expanded transverse
processes
Unmodified in males
Clavicle-interclavicle
contact
No autotomy plane
Extensiue; clavirles wide and in
contact with the interclavicular
arms for most of their length
Postxiphisternal
inscriptional ribs
Six attached, none free ( = 6 : 0) or
three attached, three free ( = 3 : 3)
KARYOTYPE
12 V +24 m (2n = 36); no sex
chromosomes (2)
Cybotoid anoles
In male only; large
Wide, on phalanges ii and iii, pad
distinctly overlaps phalanx i
Nasal modified by differentiation of
an anterior nasal which contacts the
sulcus between rostral and 1st
supralabial
7
Middorsal rows subgranular, 2 4
rows abruptly larger than flank
scales
Uniformly granular
Grade into flank scales, wide or
narrow, smooth or keeled
2 large smooth postmentals
( = sublabials) between infralabials;
always 2-4 smaller scales medial to
these
Spinulate; little intercellular
variation in spinule height and
diameter
Triangular, spatulate ( 1 )
Setal spacing typical for anoles ( I )
Smooth surface without adherent
skin
Absent in some
Ventral surface swollen and
excavated in males
Present
Labial process short
No such structures
No transverse processes; weak lateral
projections from the centra behind
the autotomy plane
Autotomy plane present
Minor; clavicles not widened, in
contact with the interclavicular
arms for not more than one-third of
length
'Two attached, two free ( = 2 : 2)
+
12 V
24 m (2n = 36); no sex
chromosomes
34 1
MOSAIC EVOLUTION IN ANOLINE LIZARDS
APPENDIX 2 continued
~~
Chamaelinorops
Cybotoid anoles
ECOLOGY
Cryptic; slow-moving; on ground or
in low vegetation (3)
Noncryptic; fast; trunk-ground in
ecology and ecomorph; A . shreuei on
ground ( 3 )
Slow high vertical head bobs with
dewlap extended (3)
Head bobs and push-ups, dewlap
extended and pulsed; details differ
among species (3)
DISPLAY