Journal of Zoology

Journal of Zoology. Print ISSN 0952-8369

Adaptation in the African egg-eating snake: a comparative

approach to a classic study in evolutionary functional
morphology
G. E. A. Gartner1,2 & H. W. Greene1
1 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA
2 Department of Biology, University of California, Riverside, CA

Keywords
Dasypeltis; egg eating; comparative methods;
Lampropeltis; selective regime; snake
feeding.
Correspondence
Gabriel E. A. Gartner, Department of
Biology, 1208 Spieth Hall, University of
California, Riverside, CA 92521, USA.
Email: ggart001@ucr.edu
Editor: Tim Halliday
Received 7 January 2008; revised 19 March
2008; accepted 20 March 2008
doi:10.1111/j.1469-7998.2008.00448.x
Abstract
A key component to any adaptive hypothesis is that the adaptive trait in question
must confer a performance advantage and, in turn, an increase in fitness, relative to
those animals displaying the phylogenetically antecedent condition. Among the most
striking purported adaptations in vertebrates are those found in the African snake
genus Dasypeltis. These snakes are unique in that they eat bird eggs to the exclusion
of all other prey. Detailed functional morphological analysis dating back 50 years
has highlighted a suite of morphological features in the head and trunk region
hypothesized to assist these animals in eating bird eggs, and yet no comparative
performance studies of egg-eating ability have ever been conducted in this group of
snakes. The purpose of this study was twofold: first, we wanted to compare egg-
eating performance in Dasypeltis with a facultative egg eater, the common king snake
Lampropeltis getula. Second, we wanted to test the hypothesis that a selective regime
exists in Africa conducive to the selection and subsequent fixation of the hypothe-
sized egg-eating morphological adaptations. Our results show that a strong advan-
tage exists in egg-eating ability for Dasypeltis. The difference is so large (only large
Lampropeltis can eat small eggs) that analysis by analysis of covariance becomes
difficult due to problems with collinearity. Our results examining potential selective
regimes show that more birds lay eggs of a readily ingestible size in Africa than in a
representative region in the United States. Additionally, the largest radiation of
African ground-nesting birds existed in Africa before the colubrid explosion during
the Miocene, which gave rise to Dasypeltis, giving further support to previous
adaptive hypotheses regarding the unique morphology of these snakes.

snakes that facultatively feed on eggs, Dasypeltis specializes

Introduction
Macrostomate snakes are among the most successful verte-
brate predators alive. They have evolved to feed on a myriad
of prey types, ranging from small invertebrates to large
mammals (Greene, 1997). Interestingly, snakes that eat
exclusively bird eggs are extremely rare (de Queiroz &
Rodrı́guez-Robles, 2006). A recent hypothesis by de Queiroz
& Rodrı́guez-Robles (2006) suggests that this paucity of
obligate egg eaters is simply due to historical contingency –
that there are relatively few snakes that supplement their
diets with bird eggs, and therefore the number of snakes that
evolved to specialize on bird eggs should be small. This
hypothesis, while accounting for important transitions in
dietary preference, does not offer support for potential
mechanisms leading to the fixation of obligate egg-eating
behavior, or the fixation of certain morphological traits
associated with egg eating.
The six species of African egg-eating snake, Dasypeltis,
eat bird eggs to the exclusion of all other prey. Unlike other
in swallowing eggs, crushing and regurgitating the shell
within the esophagus, and swallowing solely the contents.
They are unique among snakes in this regard, with the
possible exception of the Indian egg eater Elachistodon
westermanni, an extremely rare species hypothesized to eat
eggs based solely on the morphological features of a few
preserved specimens (Gans & Williams, 1954).
Dasypeltis possesses two suites of morphological features
hypothesized to be adaptive: those that circumvent the
problem of ingesting and swallowing bird eggs and those
pertaining to breaching the packaging of the egg contents
themselves once ingested (Gans, 1952, 1974). Modifications
of the quadrate, supratemporal and dentary bones, along
with a reduction in the number of teeth, are all hypothesized
to assist Dasypeltis in egg eating. In addition, anteroven-
trally pointing vertebral hypapophyses on the 17th through
38th vertebrae project into loose folds in the esophagus,
which both mechanically prevent the egg from moving
further into the gut and assist in cracking the shell and egg

368 Journal of Zoology 275 (2008) 368–374

c 2008 The Authors. Journal compilation

c 2008 The Zoological Society of London
G. E. A. Gartner and H. W. Greene
membrane (Gans, 1974). The combined effect of the struc-
tural features in the head and neck of Dasypeltis would
appear to be adaptive, allowing Dasypeltis to eat larger eggs
than other snakes of similar size.
Arnold’s (1983) Morphology ! Performance ! Fitness
paradigm provided both a conceptual and an analytical
model by which to approach the study of adaptation.
The reproductive fitness of any organism is ultimately tied
to how it performs in nature (e.g. escaping from a pre-
dator, defending territories, finding food or seeking
mates). Performance, in turn, is dependent on the syner-
gistic effect of numerous ‘suborganismal’ features, includ-
ing aspects of morphology, physiology and biochemistry.
Modern studies of adaptation (post Gould & Lewontin,
1979) are fundamentally comparative (Lauder, Leroi &
Rose, 1993; Garland & Losos, 1994; Gittleman & Luh,
1994; Losos & Miles, 1994; Larson & Losos, 1996). Thus,
demonstrating a link between purported adaptive aspects
of suborganismal traits and performance in an organism
(relative to others displaying the phylogenetically antece-
dent condition) is a critical first step in any study of
adaptation.
Interspecific comparative studies in a phylogenetic frame-
work are the only way to test hypotheses about the long-
term evolution of traits that do not fossilize (Baum &
Larson, 1991; Garland & Adolph, 1994). In this paper, we
examine potential adaptive traits in the African snake,
Dasypeltis – continuing a classic case study in contemporary
evolutionary morphology (Gans, 1974) for which, paradoxi-
cally, explicit tests of performance and adaptation have not
been published. First, we compare egg-eating performance
in Dasypeltis and an ecologically and morphologically more
generalized colubrid snake Lampropeltis getula (henceforth,
L. getula). Second, we test the selective regime hypothesis
put forth by Greene (1997) that the abundance of small
birds in Africa may play a role in the evolution of the egg-
eating morphology in Dasypeltis.
Materials and methods
Choice of an outgroup for comparison
Phylogenetic analysis of Dasypeltis using micro-complement
fixation and morphological characters (especially hemipenal
morphology and scutellation) suggests that Dasypeltis is a
monophyletic clade, sister to the rat snakes (including king
snakes) and the racers (Lopez, Maxson & Dowling, 1993;
Lopez & Maxson, 1995, 1996). The relationship between
Dasypeltis and other African colubroid snakes remains
unresolved, although Gravlund (2001) suggests a close
affinity to the Boiginae. The sister relationship between
Dasypeltis and the group that includes L. getula is conveni-
ent for adaptive comparison. Lampropeltis getula lacks the
morphological specializations of Dasypeltis and L. getula
frequently supplements its diet with eggs, making it an ideal
choice for comparative studies with Dasypeltis (Greene,
1989).
Journal of Zoology 275 (2008) 368–374

c 2008 The Authors. Journal compilation

c 2008 The Zoological Society of London
Adaptation in egg-eating snakes
Performance advantage
Ten Dasypeltis atra, wild caught in Uganda, ranging in age
from neonates to reproductive adults were acquired in May
2001 from Glades Herp Inc., Bushnell, FL. Two additional
juvenile specimens were acquired from Glades Herp Inc., in
May 2002. Data from three additional specimens (two
D. atra and one Dasypeltis scabra) were incorporated into
the analysis in January 2007. Snakes were housed individu-
ally in plastic ‘shoe box’-style containers measuring 29 
16  9 cm. The substrate consisted of either paper towels or
shredded aspen bark bedding. Water was provided ad
libitum via a ceramic water dish. The snakes were kept under
constant environmental conditions (27 1C, 53% humidity,
11 h light/13 h dark). Eggs were offered twice monthly in the
form of domestically raised quail Coturnix japonica, finch
Taeniopygia guttata, swallow Hirundo rustica or chicken
eggs (Gallus domestica) both commercially raised jumbo
and pullet eggs. Snakes were allowed to feed until satiated
(usually between two and four eggs). We used dial calipers
to measure snake head lengths on 9 September 2001 and 23
June 2002. Measurements were made by restraining the
snakes manually, and then measuring the distance between
the tip of the rostral scale and the distal tip of the quadrate
where it forms the joint with the compound bone. This
measurement was chosen because morphological evidence
suggests that the lower jaw length is the limiting aspect of
gape in snakes (Cundall & Greene, 2000). Experimental
feedings were limited to 1 month after measurement to
control for ontogenetic changes in egg-eating ability with
increased size. Experimental feeding trials consisted of
offering eggs of increasing size until the snake could no
longer eat the egg. Egg types used for experimental trials
were the same as those used for the general maintenance
diet. Egg width at its widest point and egg length were
measured before feeding. When an animal ate all the eggs in
a given class, they were next offered the smallest egg in the
next size class up (i.e. from the largest finch egg, to the
smallest available quail egg). All feeding events were re-
corded, although only the largest single egg eaten was used
for analysis.
In August 2001, four adult L. getula wild caught by H. W.
Greene near Portal, AZ, were brought into the laboratory
for feeding observations, along with a long-term captive of
the same species. King snakes were housed individually in
rack-style plastic boxes measuring 73  35  27 cm.
Shredded aspen bedding was used as a substrate. Environ-
mental and cage conditions were as noted above for Dasy-
peltis. Snake head lengths were measured in September 2001
and feeding trials began shortly thereafter. Snakes were not
fed for a period of 1 month before experimental feeding
trials to increase chances of egg predation. Snakes were then
offered quail eggs, four or five at a time, heated to the
37.7 1C incubation temperature of quail eggs and presented
in ceramic dishes. The individual L. getula were enticed to
investigate the eggs by smearing the eggs with the contents
of eviscerated thawed mice (only after refusing unscented
eggs on numerous occasions).
369
Adaptation in egg-eating snakes G. E. A. Gartner and H. W. Greene

The egg-eating performances of Dasypeltis and L. getula 30

were compared by one-way analysis of covariance (ANCOVA)
25
with jaw length as the covariate in SPSSs (Ver. 11.0 for

Egg width (mm)

Macintosh). We compared three models: a full model 20
including a dummy variable for species, jaw length and the Dasypeltis
15
product of those variables (the interaction term); a reduced
model excluding the interaction term; and a reduced model 10
including jaw size (thus describing non-parallel slopes with a L. getula
5
single intercept).
0
10 15 20 25 30 35
Selective regime Lower jaw length (mm)
Data for the analysis of selective regimes were gathered from Figure 1 Regression of maximum egg size eaten versus lower jaw
the literature (Winterbottom, 1948; Reed, 1965; Harrison, length for both Dasypeltis and Lampropeltis. Analysis of covariance
1975; Walters, 1994; Baicich & Harrison, 1997; Tarboton, results must be interpreted with caution due to the minimal overlap in
2001). Details on bird nest geographical location, habitat head size between the two species. Nevertheless, the within-species
and egg size were collected for 690 native birds known to relationships are so strong that the overall result is clear.
nest in southern Africa (the region south of the Zambezi and
Kunene rivers, comprising Namibia, Botswana, Zimbabwe,
South Africa, Lesotho, Swaziland and southern and central Table 1 Summary statistics for the three proposed regression models
Mozambique) and for 281 birds known to nest in the United
Standard error
States east of the Mississippi River. Bird nests were grouped
Model R2 of the estimate F
according to nesting habitat and location. In particular, we
Full model 0.947 1.4434 65.2
were interested in whether a significant difference existed in
Same slopes, different intercepts 0.931 1.5756 80.6
the relative abundance of eggs of an ingestible size between
Different slopes, same intercept 0.946 1.3946 104.6
those areas where Dasypeltis and L. getula are routinely
encountered. Both Dasypeltis and Lampropeltis are primar- Model 3, which excludes the interaction term, but includes jaw size, is
ily terrestrial foragers, but both will routinely enter shrub- most appropriate for our data.
bery in pursuit of prey. Therefore, we included nests in
burrows and shrubbery up to 3 m in height in the analysis
while excluding nests on floating pads in wetlands and nests Table 2 Correlation matrix of independent variables
on rocky cliff edges where these snakes are unlikely to forage
Egg radius Jaw length Species Interaction
actively for prey. We used kernel density estimates to
estimate distributions of egg sizes among only ground Egg radius 1.000 – – –
Jaw length 0.043 1.000 – –
nesters in the two regions, and again comparing all egg sizes
Species 0.593 0.815 1.000 –
for the two regions. Bandwidth was optimized using SAS/
Interaction 0.834 0.551 0.926 1.000
STATs software (SAS Institute Inc.) using the minimum
asymptotic mean integrated squared error criterion. Egg Model 1 is inappropriate for our analysis because of the extreme
sizes were not normally distributed. We used a Kruskall– correlation between the interaction term and species.
Wallis test to look for differences in mean egg size between
the two regions and a Kolmogorov–Smirnov test to examine
to the multicollinearity of the predictors, rather than any
differences in the relative distributions of egg sizes in Africa
one variable (species or jaw length) being a significant
and North America.
predictor of a snake’s ability to eat an egg of a given size.

Results Selective regime

Performance advantage
Figure 1 shows the within-species relationships in egg eating
between L. getula and Dasypeltis. All three models fit the
data (P0.01; see Table 1 for summary). However, model 3
(which assumes different slopes but the same intercept)
appears to fit best, having among the highest R2, the lowest
standard error of the estimate and the highest F value
(R2 = 0.946, SEE= 1.3592 and F = 46.6; see Table 1). The
full model is not appropriate because the interaction term
and species are too highly correlated (see Table 2). In
addition, the significant fit of the model is more likely due
Overall, there is no significant difference in the mean egg size
between the two regions, although the relative egg size dis-
tribution between the southern African and the eastern United
States is marginally significant (mean egg size eastern United
States= 24.292, mean egg size southern Africa= 23.187,
H= 2.58, P= 0.1081, D= 0.0975, P= 0.0453, see Fig. 2a).
However, when the analysis is restricted to ground-nesting
birds only, there is a highly significant difference between the
distributions of both the mean egg size and the relative egg size
in the two regions (mean egg size eastern United
States= 26.729, mean egg size southern Africa= 22.009,
H= 11.23, P= 0.0008, D=0.2414, P= 0.0009, see Fig. 2b).

370 Journal of Zoology 275 (2008) 368–374

c 2008 The Authors. Journal compilation

c 2008 The Zoological Society of London
G. E. A. Gartner and H. W. Greene Adaptation in egg-eating snakes

0.07
(a)

0.06
Southern Africa
0.05 Eastern United States
Density

0.04

0.03

0.02

0.01

0.00
0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150
Egg width (mm)

0.07
(b)

0.06
Southern Africa Figure 2 Kernel density estimates for (a) all eggs
0.05 measured and (b) ground-nesting bird eggs only
Eastern United States
in the two regions. Both the mean egg size and
Density

0.04 the relative distribution of egg sizes are signifi-

cantly different when the analysis is restricted to
0.03 ground nesters. More species lay small eggs in
southern Africa than in the eastern portion of the
0.02 United States (a) mean egg size eastern United
States=24.292, mean egg size southern
0.01 Africa=23.187, H= 2.58, P=0.1081, D= 0.0975,
P= 0.0453; (b) mean egg size eastern United
0.00 States=26.729, mean egg size southern
0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 Africa=22.009, H=11.23, P= 0.0008, D= 0.2414,
Egg width (mm) P= 0.0009.

We used our own feeding trials to estimate, roughly, the Discussion

largest egg that can be consumed by either Dasypeltis or
L. getula with a head length of 30 mm (56.19 and 16.15 mm
diameter, respectively, using our experimentally generated
regression). Using this estimate of maximum ingestible egg
size for adults of both species, we can determine the relative
percentage of eggs that can be eaten by a given species in a
specific regime. In southern Africa, Dasypeltis is capable of
eating 98% (232 of 236 species) of the eggs it encounters
while foraging on the ground or in shrubbery. Contrast this
with L. getula, which is only able to eat 36% (33 of 92
species) of ground-nesting bird eggs it encounters in the
eastern portion of the United States. Interestingly, Dasypeltis
is capable of eating 97% (89 of 92 species) in the
North American regime, while L. getula is capable of
eating roughly 49% (115 of 236 species) of ground-nesting
birds when placed hypothetically in the African regime.
The increase in the availability of eggs for L. getula when
placed in the African regime becomes significant
when discussing possible selective factors that could
lead to the fixation of adaptive traits associated with egg
eating in Dasypeltis.
Performance
Several generalist snake predators eat eggs; adult L. getula
and many members of the rat snake genera Pantherophis (de
Queiroz & Rodrı́guez-Robles, 2006) and Elaphe opportu-
nistically feed on both eggs and nestling birds (Greene,
1997). These snakes, however, have no special behavioral
or morphological features to assist them in the consumption
of eggs. The Japanese rat snake Elaphe climacophora ingests
large eggs and has several anterior-facing vertebral hypapo-
physes projecting ventrally toward the esophagus (Gans &
Oshima, 1952; Gans, 1974). However, E. climacophora
ingests the entire egg, including the shell (Gans & Oshima,
1952). Only Dasypeltis specializes in ingesting large eggs,
then crushing the shell and retaining solely the contents.
Our results show that a large performance advantage in
the consumption of bird eggs exists in Dasypeltis when
compared with a more generalized facultative egg-eating
colubrid L. getula. The suite of adaptive morphological
features clearly gives Dasypeltis an advantage when

Journal of Zoology 275 (2008) 368–374

c 2008 The Authors. Journal compilation

c 2008 The Zoological Society of London 371
Adaptation in egg-eating snakes
consuming even modestly sized eggs (such as quail eggs).
Although Gans (1952, 1974) distinguished between the
adaptive features of Dasypeltis that pertain to swallowing
and those that assist in manipulating the food item for
packaging in the gut, it is the combined effect of the features
that leads to the dramatic increase in swallowing ability. Our
observations of generalist snakes (Elaphe obsoleta, L. getula)
attempting to swallow eggs have shown that, even for small
eggs, the snakes often struggle with the initial ingestion, with
the egg tending to roll and slip out of the mouth. In addition,
swallowing the egg after it has passed the distal tips of the
quadrate seems to pose significantly more problems for
generalist snakes than it does for Dasypeltis. In stark contrast,
Dasypeltis can not only eat massive eggs relative to its head
size, but it does so – at least qualitatively – with relative ease.
A consequence of elongation in snakes is a reduction in
head size relative to their bodies. Macrostomate snakes are
thus forced to ingest few, but relatively massive prey items
(compared with their heads). Incompressible and slippery
prey items, such as eggs, pose special mechanical problems
during feeding in snakes (Gans & Oshima, 1952; Gans,
1974; Greene, 1997). The pterygoid walk (Cundall, 1983),
associated with feeding in many macrostomates, is ill suited
to moving large eggs through the oral cavity, resulting in
forces that tend to move eggs out of the mouth rather than
down the esophagus. It seems then that most facultative egg
eaters must eat numerous small eggs if they are going to
meet their energetic needs. Thus, while eggs may be an
opportunistic ‘treat’ of sorts, they are not effective as a
primary diet in most instances.
The comparative study and demonstration of a perfor-
mance advantage lends further support to Gans’ initial
adaptive hypothesis. Further substantiation of adaptive
claims comes from rejection of non-adaptive hypotheses
(Baum & Larson, 1991; Larson & Losos, 1996) because the
character may be present as a developmental artifact (Gould
& Lewontin, 1979) or as a retained feature that no longer
confers an advantage in extant lineages (Greene, 1986). In
this study, the possibility of allometric artifacts (Carothers,
1986) can be rejected because the presence of structural
modifications, particularly in the skull of Dasypeltis, is
independent of both size and age (although see Gans, 1952,
1974 for a complete discussion). The structural modifica-
tions of Dasypeltis are a derived feature of the genus (Lopez
et al., 1993), as are the extreme modifications of the
vertebral hypapophyses (cf. Gans & Oshima, 1952, for a
comparison with E. climacophora), and so they cannot be
the retained vestiges of a primitive character. This leaves
adaptive hypotheses as the most probable explanation.
The two sets of adaptations, in both the head and the
vertebrae, work in concert, allowing Dasypeltis to not only
eat enormously large eggs but, by crushing and regurgitating
the eggshell, the snakes minimize the volume the eggs take
up in the gut. Although the difference in egg-eating ability is
dramatic, the results must be interpreted with caution due to
the small sample size, particularly with L. getula. Further-
more, as shown in Fig. 1, the data indicate that there is only
a minor region of overlap between the dependent variable
372 Journal of Zoology 275 (2008) 368–374

c 2008 The Authors. Journal compilation

G. E. A. Gartner and H. W. Greene
(maximum egg size consumed) and the covariate (jaw
length) between species. Only large Lampropeltis can eat
small eggs, whereas the maximum lower jaw length of even
large Dasypeltis just approaches that of our egg-eating king
snakes. Therefore, all ANCOVA models must be interpreted
with caution. Nevertheless, the within-species relationships
are so strong that the overall result is clear. Further
examination of museum specimens of L. getula with eggs in
their stomachs would allow us to further quantify the
performance advantage between Dasypeltis and L. getula.
Selective regime
Our data demonstrate that a potential selective regime exists in
southern Africa that is conducive to the fixation of adaptive
traits associated with egg eating within ancestral populations of
Dasypeltis. The high incidence of ground-nesting birds provides
the environmental context for the evolution of features that
confer a performance advantage associated with egg eating.
Demonstrating the presence of a selective regime – along
with a performance advantage and rejection of non-adap-
tive hypotheses – fulfills a third requirement in claiming
adaptation of a particular set of morphological or behavior-
al features (Baum & Larson, 1991; Larson & Losos, 1996).
Larson & Losos (1996) point out that a critical component
of the selective regime in inferring adaptation is that it must
arise in unison with the organismal feature being studied –
traditionally carried out by mapping the origin of the
proposed regime onto a phylogenetic tree. Mapping charac-
ters may be possible with broadly defined regimes, such as
‘arboreality.’ However, in highly specified regimes, such as
the one in this study, it is nearly impossible. The avian
families Fringillidae and Estrildidae are among the most
diverse and speciose lineages African bird faunas. These birds
consist of small finches and weaverbirds that probably make
up the bulk of Dasypeltis’ diet. The African radiation of these
birds is estimated to have occurred roughly 24–26 million
years ago (Barker et al., 2004) while the colubrid explosion –
which would include Dasypeltis – is thought to have occurred
during the Miocene, 5–25 million years ago (Greene, 1997).
These dates indicate that, at a minimum, the ancestral snakes
that gave rise to Dasypeltis evolved concurrently with the
massive radiation of small African birds that could provide
ample food for an obligate egg-eating predator.
More work can certainly be done on the selective regime
for egg-eating adaptations of snakes. Other aspects of
ecology, such as competition and prey density, may play a
role in the evolution of adaptive traits. Species number says
nothing of population density, which would be a more
accurate test of egg abundance. However, nest density data
for such a large number of species over such a broad
geographic range are lacking. Therefore, species number
must be used as a first-order approximation of egg avail-
ability. We have examined only a small sample of the
available biota in only two geographic regions. Further tests
of the hypothesis would entail examining bird faunas in
other regions of the world (Europe, Asia, South America
and Australia).
c 2008 The Zoological Society of London
G. E. A. Gartner and H. W. Greene
Acknowledgments
The presentation of this paper was improved by helpful
comments from K.R. Zamudio, R.W. Clark and J.S.
Rodrı́guez of Cornell University, J.C. O’Reilly of the Uni-
versity of Chicago, A. Savitzky of Old Dominion University
and by T. Garland, M. Turcotte and Brooke ‘Keen Bean’
Keeney of the University of California, Riverside. Addition-
ally, the authors wish to thank A. Herrel of the University of
Antwerp for his comments and data on three Dasypeltis.
T. Phillipi of Florida International University was especially
helpful with the interpretation of selective regime data. K.D.
Wiseman generously donated data on egg eating in
L. getula. Special thanks are due to E. Adkins-Regan,
J. Schuetz, A. Hand and B. Berggren-Thomas of Cornell
University for their donation of various eggs and to John
Friel at the Cornell Museum of Vertebrates for data collec-
tion on L. getula. Portions of the analyses for this paper
were generated using SAS/STAT software, Version 9.1.3 of
the SAS system for UNIX. Copyright 2002–2006. SAS
Institute Inc. SAS and all other SAS Institute Inc. product
or service names are registered trademarks or trademarks of
SAS Institute Inc., Cary, NC, USA.
References
Arnold, S.J. (1983). Morphology, performance and fitness.
Am. Zool. 23, 347–361.
Baicich, P.J. & Harrison, C.J.O. (1997). A guide to the nests,
eggs, and nestlings of North American birds. San Diego:
Academic Press Inc.
Barker, F.K., Cibois, A., Schikler, P., Feinstein, J. & Cracraft,
J. (2004). Phylogeny and diversification of the largest avian
radiation. Proc. Natl. Acad. Sci. USA 101, 11040–11045.
Baum, D.A & Larson, A. (1991). Adaptation reviewed: a
phylogenetic methodology for studying character macro-
evolution. Syst. Zool. 40, 1–18.
Carothers, J.H. (1986). An experimental confirmation of
morphological adaptation: toe fringes in the sand-dwelling
lizard Uma scoparia. Evolution 40, 871–874.
Cundall, D. (1983). Activity of head muscles during feeding
by snakes: a comparative study. Am. Zool. 23, 383–396.
Cundall, D. & Greene, H.W. (2000). Feeding in snakes. In
Feeding: form, function, and evolution in Tetrapod verte-
brates: 293–333. Schwenk, K. (Ed.). San Diego: Academic
Press.
Gans, C. (1952). The functional morphology of the egg-eating
adaptations in the snake genus Dasypeltis. Zoologica 37, 209.
Gans, C. (1974). Biomechanics: an approach to vertebrate
biology. Ann Arbor: The University of Michigan Press.
Gans, C. & Oshima, M. (1952). Adaptations for egg eating in
the snake Elaphe climacophora (Boie). Am. Mus. Nov. 1571,
1–16.
Gans, C. & Williams, E.E. (1954). Present knowledge of the
snake Elachistodon westermanni (Reinhardt, 1863). Bre-
viora: Mus. Comp. Zool. 36, 1–17.
Journal of Zoology 275 (2008) 368–374

c 2008 The Authors. Journal compilation

c 2008 The Zoological Society of London
Adaptation in egg-eating snakes
Garland, T. Jr. & Adolph, S.C. (1994). Why not to do two-
species comparative studies: limitations on inferring adap-
tation. Physiol. Zool. 67, 797–828.
Garland, T. Jr. & Losos, J.B. (1994). Ecological morphology
of locomotor performance in squamate reptiles. In Ecolo-
gical morphology: integrative organismal biology: 240–303.
Wainright, P.C. & Reilly, S.M. (Eds). Chicago, IL: Uni-
versity of Chicago Press.
Gittleman, J.L. & Luh, H.K. (1994). Phylogeny, evolutionary
models and comparative methods: a simulation study. In
Phylogenetics and ecology: 103–122. Vane-Wright, R.I.
(Ed.). San Diego: Academic Press.
Gould, S.J. & Lewontin, R. (1979). The spandrels of San
Marcos and the panglossian paradigm: a critique of the
adaptationist programme. Proc. Roy. Soc. Lond. Ser. B:
Biol. Sci. 205, 581–598.
Gravlund, P. (2001). Radiation within the advanced snakes
(Caenophidia) with special emphasis on African opisto-
glyph colubrids, based on mitochondrial sequence data.
Biol. J. Linn. Soc. 72, 99–114.
Greene, H.W. (1986). Diet and arboreality in the Emerald
Monitor, Varanus prasinus, with comments on the study of
adaptation. Fieldiana 31, 1–12.
Greene, H.W. (1989). Ecological, evolutionary, and conser-
vation implications of feeding biology in old world cat
snakes, genus Boiga (Colubridae). Proc. Calif. Acad. Sci.
46, 193–207.
Greene, H.W. (1997). Snakes: the evolution of mystery in
nature. Berkeley: University of California Press.
Harrison, H.H. (1975). A field guide to the birds’ nests: United
States east of the Mississippi river. Boston: Houghton
Mifflin.
Larson, A. & Losos, J.B. (1996). Phylogenetic systematics of
adaptation. In Adaptation: 187–220. Lauder, G.V. & Rose,
M. (Eds). San Diego: Academic Press.
Lauder, G.V., Leroi, A.M. & Rose, M.R. (1993). Adaptations
and history. Trends Ecol. Evol. 8, 294–297.
Lopez, T.J. & Maxson, L.R. (1995). Mitochondrial DNA
sequence variation and genetic differentiation among Co-
lubrine snakes (Colubridae: Colubrinae). Biochem. Syst.
Ecol. 23, 487–505.
Lopez, T.J. & Maxson, L.R. (1996). Albumin and mitochon-
drial DNA evolution: phylogenetic implications for co-
lubrine snakes (Colubridae: Colubrinae). Amphibia-
Reptilia 17, 247–259.
Lopez, T.J., Maxson, L.R. & Dowling, H.G. (1993). Phylo-
genetic relationships of the African egg-eating snake,
Dasypeltis scabra. Amphibia-Reptilia 14, 223–236.
Losos, J.B. & Miles, D.B. (1994). Adaptation, constraint, and
the comparative method: phylogenetic issues and methods.
In Ecological morphology: integrative organismal biology:
60–98. Wainright, P.C. & Reilly, S.M. (Eds). Chicago:
University of Chicago Press.
de Queiroz, A. & Rodrı́guez-Robles, J.A. (2006). Historical
contingency and animal diets: the origins of egg eating in
snakes. Am. Nat. 167, 684–694.
373
Adaptation in egg-eating snakes G. E. A. Gartner and H. W. Greene

Reed, C.A. (1965). North American bird eggs. Toronto: Dover
Publications Inc.
SAS Institute Inc. (2000-2004). SAS 9.1.3 help and documen-
tation. Cary, NC: SAS Institute Inc.
SPSS Inc. (2002). SPSS 11.0 for Macintosh. Chicago, IL:
SPSS Inc.
Tarboton, W. (2001). A guide to the nests and eggs of Southern
African birds. Cape Town: Hirt and Carter Ltd.
Walters, M. (1994). Birds’ eggs. New York: Dorling Kinderley
Inc.
Winterbottom, J.M. (1948). Priest’s eggs of Southern African
birds. Johannesburg: Winchester Press.

374 Journal of Zoology 275 (2008) 368–374

c 2008 The Authors. Journal compilation

c 2008 The Zoological Society of London