AMER. ZOOL., 20:351-362 (1980)
Evolution of the Cleidoic Egg Among Reptilian
Antecedents of Birds 1
GARY C. PACKARD AND MARY J. PACKARD
Department of Zoology and Entomology,
Colorado State University, Fort Collins, Colorado 80523
SYNOPSIS. Evolution of the avian egg from the naked, amniotic egg of ancestral reptiles
probably was the outcome of intense predation by soil invertebrates and microbes on a
highly integrated and coadapted complex of characters. The calcareous shell, which from
its inception afforded a measure of protection to eggs against attacks by soil organisms,
became progressively thicker and more complex in the face of continuing selection for
antipredator devices. However, increases in thickness and complexity of eggshells led to
simultaneous reductions in the amount of liquid water that could be absorbed by incubating eggs from the substrate. Because embryos initially were dependent upon uptake
of substantial quantities of water from the environment to satisfy their needs for this
solvent, adaptive increases in thickness of the eggshell required coupled increases in the
amount of water contained by eggs at oviposition, thereby reducing the degree of dependence of embryos upon external sources of water for successful completion of development. The rigid-shelled eggs resulting from this evolutionary sequence absorbed little (if
any) liquid water during incubation, and the eggs contained sufficient water at oviposition
to sustain embryos to hatching. Such eggs were functionally cleidoic and had attained an
avian level of organization.
INTRODUCTION
Our objectives in this essay are (1) to
propose a plausible conceptual model accounting for the evolution of cleidoic eggs2
among the reptilian progenitors of birds,
and (2) to illustrate how studies of eggs of
contemporary reptiles can contribute new
insights concerning this important evolutionary event. The evolutionary model formulated here represents a refinement of
ideas presented first by Gray (1928) and
Needham (1931); and while this model is
not the only one that could be proposed,
it does satisfy the requisite of being consistent with the meager body of evidence
presently available.
EGGS OF EARLY REPTILES
After examining the skeletal morphology of Paleozoic amphibians and reptiles
and comparing it with that of contemporary forms, the paleontologist Robert Carroll (1970) proposed that the earliest reptiles—the romeriid captorhinomorphs
1
From the Symposium on Physiology of the Avian
Egg presented at the Annual Meeting of the American Society of Zoologists, 27-30 December 1979, at
Tampa, Florida.
2
A cleidoic egg is one whose "walls . . . can only be
penetrated by matter in the gaseous state" (Needham,
1931).
from the Lower Pennsylvanian—reproduced by way of relatively naked amniotic
eggs capable of undergoing direct development in terrestrial settings, in much the
same manner as occurs today in many salamanders of the family Plethodontidae
(see Salthe, 1969). Because there presumably was no free-living larval stage, eggs of
these early reptiles probably contained a
large mass of yolk, thereby providing the
necessary energy reserves to sustain embryos through the prolonged egg-stage to
hatching. Several thin layers of jelly may
have encased the yolk and embryo, the
outermost layer being dense, tough, and
resistant to abrasion (see Salthe, 1963) and
the inner layers being more jelly-like and
watery. The outermost of the jelly capsules
may have constituted a forerunner of the
shell membrane, and the inner layers of
albumen (see Gray, 1928; Needham,
1931).
Although eggs of the earliest reptiles
probably were not deposited in standing
water, it is likely nevertheless that sites selected by females for oviposition (e.g., subterranean chambers, spaces beneath objects on the surface of the ground, etc.)
were very wet and that eggs could exchange water freely with the saturated soil
(see Heatwole, 1961; Salthe and Mecham,
352
G. C. PACKARD AND M. J. PACKARD
1974). Indeed, because eggs probably did
not contain sufficient water at the time of
deposition fully to satisfy requirements of
embryos for this solvent, the absorption of
liquid from the substrate may have been
essential for successful completion of embryogenesis (see Gray, 1928; Needham,
1931).
Eggs of the earliest reptiles must therefore have differed strikingly from those of
contemporary birds (see Romanoff and
Romanoff, 1949), with one of the more
obvious differences being the absence of
a calcareous shell from eggs of the Pennsylvanian reptiles. However, eggs of contemporary reptiles exhibit a broad spectrum in the degree of development of the
shell layer (Agassiz, 1857; Giersberg, 1922;
Erben, 1970; G. C. Packard et al., 1977;
Ewert, 1979; Sexton et al., 1979), effectively bridging the gap between the naked
eggs of ancestral reptiles and those of living birds. While we do not suggest that the
eggs of contemporary reptiles are "primitive," we do believe that they are less differentiated from the apparent ancestral
form (at least with respect to the shell) than
are the eggs of contemporary birds. Thus,
important insights can be gained from
close examination of eggs of extant reptiles
concerning stages through which eggs
must have passed during the evolution of
present-day birds.
Eggs of oviparous lizards, snakes, and
other lepidosaurians depart only slightly
from the presumed ancestral form. A
large mass of yolk is enclosed by a thin
layer of albumen (Dendy, 1899; Clark,
1946), external to which is a multi-layered
shell membrane (Dendy, 1899; G. C. Packard et al., 1977; Sexton et al., 1979). In
eggs of some species, no discrete shell layer
is evident, and much of the surface of the
shell membrane appears to be naked and
exposed to the environment (Giersberg,
1922; Kriesten, 1975; Sexton et al., 1979).
In eggs of other species, however, a thin
crust of calcareous matter lies on the surface of the shell membrane (Dendy, 1899),
this crust being formed of crystalline material—presumably calcium carbonate—
arranged in an open, unstructured matrix
(Fig. 1A, B). Because lepidosaurian eggs
lack a highly structured shell layer, the
shell membrane can easily be stretched
and deformed without damaging the egg.
Indeed, this capacity for deformation and
stretching probably is a critical factor in
enabling eggs to absorb relatively large
quantities of water from the substrate (see
beyond), for eggs may increase appreciably in volume in consequence of water absorption (see G. C. Packard et al., 1977).
Pliable-shelled eggs of many species of
turtles (e.g., sea turtles, chelydrids, most
emydids) are intermediate between the
presumed ancestral condition and that of
eggs of contemporary birds. A large mass
of yolk is surrounded by a relatively thick
layer of albumen, over which lies a single,
multi-layered shell membrane (Solomon
and Baird, 1976; M. J. Packard, 1980).
Eggs of sea turtles have a calcareous shell
resembling in certain respects that found
in eggs of some lepidosaurians (Fig. 1C,
D), inasmuch as the crystals of calcium carbonate are randomly arranged to form a
rather open matrix (Solomon and Baird,
1976; Baird and Solomon, 1979). The
crystalline material in eggshells of chelydrids (Fig. 2A, B) and emydids, however,
is organized into discrete shell units whose
inner tips are firmly attached to the underlying shell membrane and whose lateral
surfaces frequently make contact with
those of neighboring shell units (M. J.
Packard, 1980). In all pliable-shelled eggs,
numerous channels and pores penetrate
the shell layer (Fig. 1C, 2A), and it is
through these channels that respiratory
gases and water presumably pass. These
eggs may absorb liquid water from the substrate and therefore swell during incubation, but constraints imposed by the more
highly structured shell layer prevent the
shell membrane from stretching to the degree seen in lepidosaurian eggs (see M. J.
Packard, 1980). Thus, water absorption by
the turtle eggs is not as pronounced as occurs in eggs of lepidosaurians generally
(see beyond).
Rigid-shelled eggs of other turtles (e.g.,
trionychids, testudinids) and of crocodilians are comparable in many respects to
those of birds (Erben, 1970; G. C. Packard
et al., 1977). A large mass of yolk is sur-
EVOLUTION OF AVIAN EGGS
353
FIG. 1. A, outer surface of shell of a parchment-shelled egg of a zebra-tailed lizard (Callisaurus draconoides),
x220; B, higher magnification view of outer surface of lizard eggshell, showing details of the calcareous crust,
xl 100; C, outer surface of shell of a pliable-shelled egg of a sea turtle (Lepidochelys kempi), X220; D, higher
magnification view of a portion of 1C, showing details of the calcareous matrix, X450.
354
G. C. PACKARD AND M. J. PACKARD
FIG. 2. A, outer surface of shell of a pliable-shelled egg of a snapping turtle (Chelydra serpentina), showing
loosely arranged shell units and a large number of pores, xl 10; B, radial view of snapping turtle eggshell,
showing single shell membrane and shell units that are firmly attached to the outer surface of the membrane,
xl 10; C, outer surface of shell of a rigid-shelled egg of a softshell turtle (Trionyx spiniferus), showing that shell
units are tightly wedged against one another and that shell is penetrated by relatively few pores, xllO; D,
radial view of softshell turtle eggshell; inner and outer shell membranes are visible; shell units arise from
sites of nucleation on the outer surface of the outer shell membrane, X250.
EVOLUTION OF AVIAN EGGS
rounded by a thick envelope of albumen,
external to which is a pair of shell membranes (Reese, 1915; Bigalke, 1931; Young,
1950; Erben, 1970; M. J. and G. C. Packard, 1979). The calcareous shell (Fig. 2C,
D), which is as thick as in avian eggs of
comparable size (G. C. Packard et al.,
19796), is formed of tightly packed shell
units arising from sites of nucleation on
the outer shell membrane (Erben, 1970;
M. J. and G. C. Packard, 1979). The mineral layer occasionally is interrupted by
pores (Fig. 2C) which apparently provide
for the exchange of gases and water between the contained embryo and the surrounding environment (Young, 1950; Erben, 1970; M. J. and G. C. Packard, 1979).
The interlocking of crystallites of adjacent
shell units renders the calcareous layer rigid and non-compliant. Although eggs such
as these can absorb liquid water from the
substrate (see beyond), the quantities absorbed seem generally to be very small,
and on those occasions when appreciable
uptake occurs, the mineral layer becomes
cracked and disrupted (Plummer, 1976;
Webb etal., 1977.
Thus, eggs of living reptiles fall conveniently into one of three categories based
upon the degree of development of the
calcareous shell: (1) eggs with highly extensible shells exhibiting minimal development of the mineral layer, (2) eggs with
moderately extensible shells characterized
by a more highly structured mineral layer,
and (3) eggs with nonextensible shells comprised of a highly organized and structured mineral layer. Consideration of the
eggs of oviparous lepidosaurians can provide insights pertaining to early stages in
the development of avian eggs, and examination of pliable-shelled eggs of turtles
can yield new understanding of intermediate stages in this evolutionary event. Finally, rigid-shelled eggs of turtles and
crocodilians can easily be regarded as having attained an avian level of organization,
and may therefore contribute to an understanding of the conditions under which
eggs of the very earliest birds developed.
SELECTION FOR A SHELL LAYER
Living reptiles generally deposit their
eggs in subterranean chambers or other
355
sheltered sites where the humidity is high
(Tracy et al, 1978; G. C. Packard et al,
1979a) and the temperature moderate (G.
C. Packard et al, 1977). During the course
of incubation, however, the eggs are vulnerable to attack by a variety of organisms.
Ants (e.g., Moll and Legler, 1971; Burger,
1977), larval dipterans (e.g., Cagle, 1937),
and other invertebrates may consume the
contents of eggs, and the antimicrobial
property of albumen (Movchan and Gabaeva, 1967; see also Ewert, 1979) is indirect evidence of the danger posed to
embryos by bacteria, molds, and fungi.
Depredations by these organisms may
be a major source of mortality in natural populations (see Moll and Legler,
1971), so selection for antipredator mechanisms frequently is high.
Assuming that eggs of ancestral reptiles
also were subjected to predation by invertebrates and to invasion by microbes, it is
possible that the calcareous layer had its
inception as a defense mechanism. The
shell of avian eggs is a non-specific protection against such attacks, and effectiveness
of the calcareous layer in affording protection to the yolk and embryo is related
directly to its thickness and inversely to its
apparent porosity (Board and Fuller,
1974). Crocodilian eggs suffering severe
cracks are seemingly more susceptible to
invasion by microorganisms than intact
eggs (see Webb et al, 1977; Goodwin and
Marion, 1978), further indicating the possible role of the shell as an antipredator
device.
Among early reptiles ancestral to birds,
those females laying eggs exhibiting some
degree of calcification of the shell membrane may have given rise to more hatchlings than conspecifics producing eggs
having little or no calcification of the membrane, owing to the slight advantage the
calcareous material conferred as a protection against attack by insects and microorganisms. Continued selection exerted
through soil invertebrates and microbes
could have led to progressive increases in
thickness and complexity of the shell layer,
which presumably passed through a series
of stages similar to those described previously for eggs of contemporary reptiles
before arriving at the avian condition.
356
G. C. PACKARD AND M. J. PACKARD
owing to reductions in the number of
pathways available for capillary transport
of water through the shells and to in190
creases in the length of these pathways;
180
and increases in resistance of eggshells to
water transport must have led in turn to
• Callisaurus draconoides
170
reductions in the total amount of water
1
Chelydra serpentina
that could be absorbed by eggs during in•
Trionyx spiniferus
g 160
cubation. This point can be illustrated by
UJ
comparing eggs of contemporary reptiles
8 150
exhibiting different degrees of developo
ment of the calcareous layer.
•I 140
Temporal changes in mass of incubating
reptilian eggs are complex (Fig. 3), because
° 130
eggs absorb liquid water across that part of
their shell contacting the substrate while
120
simultaneously exchanging vapor across
that part of their shell exposed to air
110
trapped inside the nest chamber (Tracy et
al., 1978; G. C. Packard et al., unpub100
lished). However, influx of liquid from the
substrate
seems to have its greatest effect
25
50
75
100
on changes in mass of eggs during the first
% of Incubation Completed
half of incubation (G. C. Packard et al.,
FIG. 3. Eggs of the lizard Callisaurus draconoides, the
turtle Chelydra serpentina, and the turtle Trionyx spi-unpublished), so changes in mass of eggs
niferus were half-buried in vermiculite having water during the first weeks of incubation can be
potentials of - 100 kPa, -130 kPa, and - 5 0 kPa, re- taken as a convenient index to the conspectively. The percent of original mass of eggs is ductance of eggshells to liquid water.
plotted in relation to the percent of incubation that
When incubated with half of their surhad been completed.
face in contact with vermiculite having a
water potential of approximately - 1 0 0
kPa,3 parchment-shelled eggs of zebraCONSEQUENCES OF ACQUIRING A SHELL
tailed lizards (Callisaurus draconoides) nearUptake of waterfront soil
ly double in mass during the first 2 weeks
As indicated earlier, eggs of ancestral of a 33-day period of incubation (Fig. 3),
reptiles probably were deposited on wet whereas pliable-shelled eggs of snapping
substrates, where the water potential of the turtles (Chelydra serpentina) increase in mass
soil was higher than that of the contents of by about 15% during a comparable intereggs themselves. This difference in water val (Fig. 3). In contrast, rigid-shelled eggs
potential must have promoted the flow of of softshell turtles (Trionyx spiniferus) exwater from the substrate into eggs (see G. hibit little (if any) change in mass during
C. Packard etal, 1977; Tracy etal, 1978), the first half of incubation, even when inwith the rate of influx of liquid being in- cubated on vermiculite slightly wetter than
fluenced also by the amount of surface that used for incubating eggs of the other
contacting the substrate (Tracy et al., 1978; species (Fig. 3). Thus, conductance of eggM. J. Packard et al., unpublished) and by shells to water appears to be highest in
the conductance of eggshells to liquid eggs exhibiting minimal development of
water (see G. C. Packard etal., 1977; Tracy the calcareous layer and lowest in eggs
having highly organized shells.
etal., 1978).
Evolutionary increases in thickness and
complexity of reptilian eggshells must
3
have led to parallel increases in resistance
A water potential of — 100 kPa in the Internationof eggshells to transport of liquid water, al System of Units is equal to - 1 bar.
200
EVOLUTION OF AVIAN EGGS
357
TABLE 1. Mean mass of zebra-tailed lizards ( Callisaurus
draconoides) hatching from parchment-shelled eggs incubated at 35°C on the surface of substrates differing slightly
in water potential. *
Substrate water
potential (kPa)
Hatchling mass
(mg)
Sample size
-100
-200
798.8
704.4
7
14
* Values for individual hatchlings were adjusted by
analysis of covariance (Snedecor and Cochran, 1967)
to compensate for differences in size of animals stemming from differences in the size of eggs in which
development occurred. The Least Significant Difference (Snedecor and Cochran, 1967) at a probability
of 0.05 is 69.0 mg. Substrate water potentials were
measured by thermocouple psychrometry (Brown
and Van Haveren, 1972).
Importance of water uptake
Prior to the evolutionary appearance of
calcareous material on the surface of the
shell membrane, eggs of ancestral reptiles
probably exchanged water freely with the
environment, and a substantial portion of
the water required to sustain embryonic
development probably was obtained from
outside the egg (see Gray, 1928; Needham,
1931). Because evolutionary development
of the eggshell must have led to progressive reductions in the amount of water that
could be absorbed by incubating eggs from
the substrate, it is therefore likely that increases in thickness and complexity of eggshells were accompanied by decreases in
the reliance of developing embryos upon
external sources of water.
Embryos of contemporary reptiles vary
in their apparent dependence upon external sources of water, and this variation is
related to the degree of development of
the eggshell. For instance, lizard embryos
developing inside parchment-shelled eggs
are highly dependent upon external
sources of water for successful completion
of embryogenesis (M. J. Packard etal., unpublished). Substantial amounts of water
absorbed from the substrate are incorporated into the protoplasm of developing
embryos (Tracy, 1980; M. J. Packard et
al., unpublished), and eggs incubated on
substrates no drier than —300 kPa exhibit
extraordinarily low hatching success (Fig.
4). Even when eggs are incubated on sub-
-100
-200
-340
-450
Substrate Water Potential (kPa)
FIG. 4. Hatching success for parchment-shelled eggs
of the lizard Callisaurus draconoides incubated on the
surface of substrates differing in water potential.
Vertical lines define 95% confidence intervals, and
the number of eggs incubated on each substrate is
given above the appropriate bar of the histogram.
Substrate water potentials were measured by thermocouple psychrometry (Brown and Van Haveren,
1972).
strates wet enough for high hatching successes to be realized, eggs held on the wettest substrates (e.g., —100 kPa) give rise to
larger hatchlings than eggs placed on
slightly drier ( — 200 kPa) substrates (Table
1). Because large hatchlings have higher
probabilities of surviving than small hatchlings do (Ferguson and Bohlen, 1978; Fox,
1978), even small differences in wetness of
the substrate between nesting sites can be
biologically significant.
Absorption of water by pliable-shelled
eggs of turtles seems not to be essential for
successful completion of embryonic development, for there is no apparent relationship between hatching success of eggs held
on wet and on relatively dry substrates
(Tracy et al., 1978; G. C. Packard et al,
unpublished). Nevertheless, the uptake of
water by eggs may have adaptive value (G.
358
G. C. PACKARD AND M. J. PACKARD
TABLE 2. Mean values for two different indices to size of
turtles hatching from pliable-shelled eggs incubated at 29°C
while half-buried in substrates differing in water potential. *
Substrate water potential (kPa)
-375
Species/variable
4.142
24.47
12
3.939
24.06
3.543
23.15
10
Chelydra serpentina
Mass (g)
(LSD = 0.209)
Carapace length (mm)
(LSD = 0.68)
Sample size
6.835
26.48
13
6.137
25.26
10
Substrate water
potential (kPa)
Hatchling mass
(g)
Sample size
-50
-450
-850
7.167
7.176
7.132
9
10
9
-610
Chrysemys picta
Mass (g)
(LSD = 0.278)
Carapace length (mm)
(LSD = 0.79)
Sample size
TABLE 3. Mean mass of softshell turtles ("frionyx spiniferus,) hatching from rigid-shelled eggs incubated at 29°C
while half-buried in substrates differing in water potential. *
5.577
25.14
12
* Values for individual turtles were adjusted by
analysis of covariance (Snedecor and Cochran, 1967)
to compensate for differences in size of animals stemming from differences in size of eggs in which development occurred. The LSD is the Least Significant
Difference (Snedecor and Cochran, 1967) at a probability of 0.05. Substrate water potentials were measured by thermocouple psychrometry (Brown and
Van Haveren, 1972).
C. Packard et al., unpublished). The
amount of water available inside pliableshelled eggs at the time of oviposition
seems not to be sufficient to allow developing embryos fully to use available energy reserves in formation of new tissue.
Thus, embryos developing in eggs absorbing relatively large quantities of water
from the substrate are able to supplement
the water already available to them in the
yolk and albumen, use available energy reserves more completely in formation of
new tissue, and grow larger before hatching than embryos developing in eggs absorbing lesser amounts of water during incubation (Table 2). Large hatchlings
probably are competitively superior to
small hatchlings and may grow more rapidly in the period following hatching than
smaller animals do (Froese and Burghardt,
1974), and survival of large hatchlings is
greater than that of smaller animals
(Swingland and Coe, 1979). Thus, water
absorption by pliable-shelled eggs—while
not of life or death importance—has apparent adaptive value.
* Values for individual turtles were adjusted by
analysis of covariance (Snedecor and Cochran, 1967)
to compensate for differences in size of animals stemming from differences in the size of eggs in which
development occurred. The Least Significant Difference (Snedecor and Cochran, 1967) at a probability
of 0.05 is 0.129 g. Substrate wa'er potentials were
estimated from the standard curve reported by Tracy
etal. (1978).
Rigid-shelled eggs of turtles may absorb
a small amount of liquid during incubation
(G. C. Packard et al., 1979a), but this uptake of liquid has no apparent importance
to developing embryos. Both hatching success (G. C. Packard et al., 1979a) and size
of emergent hatchlings (Table 3) are independent of the wetness of substrates
with which eggs are associated during incubation, indicating that embryos do not
rely upon uptake of water from the environment for completion of embryogenesis
or for making full use of available energy
reserves in formation of new tissue.
Thus, embryos of contemporary reptiles
developing inside eggs exhibiting minimal
development of the shell layer are unable
to complete embryogenesis unless large
quantities of water are taken up from the
substrate. In contrast, embryos developing
inside eggs with pliable shells benefit from
water absorption, but the water is not essential for successful completion of development. Finally, embryos developing inside eggs with rigid, highly structured
shells are completely independent of external sources of water.
Water content of eggs
It follows from the preceding discussion
that reductions in the dependence of developing embryos of ancestral reptiles
upon outside sources of water must have
been accompanied by increases in the
amount of water available inside eggs at
the time of oviposition. This contention
359
EVOLUTION OF AVIAN EGGS
TABLE 4. Water content of pliable-shelled eggs of turtles.
Species
(# of eggs?# of clutches)
Mass of eggs
(g) at
oyiposition
(X ± SD)
Water content as
% of original
mass (X ± SD)
Chelydra serpentina
(4/1)
9.75 ± 0.21
70.15 ± 1.76
Chrysemys picta
(15/5)
6.43 ± 0.34
72.18 ± 1.13
Terrapene Carolina
(4/2)
9.83 ± 0.59
67.90 ± 2.25
receives support from published accounts
of the water content of eggs of contemporary reptiles and from our own unpublished findings on the subject. For instance, oviducal eggs of lizards and snakes
vary in water content from 39-69% of
fresh mass, averaging about 56% (Ballinger and Clark, 1973; Vitt, 1974, 1978),
whereas about 70% of the mass at oviposition of pliable-shelled eggs of turtles is
water (Table 4; also Cunningham and
Hurwitz, 1936; Ricklefs and Burger,
1977). Interestingly, the rigid-shelled eggs
of softshell turtles also contain 70% water
at the time of laying ( G. C. and M. J. Packard, unpublished), and eggs of precocial
land birds are approximately 73% water
by initial mass (Romanoff and Romanoff,
1949). Thus, freshly laid eggs of several
species of turtles contain water reserves
exceeding those present in lepidosaurian
eggs and approaching (or equaling) those
•present in the aforementioned avian eggs.
Extrapolating these findings to eggs of
ancestral reptiles leads to the conclusion
that major increases in water content of
eggs accompanied early stages in the evolutionary development of the eggshell, but
that little further increase in water content
occurred once an organized shell layer had
appeared. Thus, in early stages of the evolution of the avian egg, provision of additional water apparently was of major importance, whereas in late stages in the
sequence, conservation of available water
may have taken precedence (see beyond).
TABLE 5. Comparison of empirically determined values for
water-vapor conductance of reptilian eggs with values predicted for avion eggs of comparable size. *
Species
Chelydra
serpentina
Trionyx
spiniferus
Alligator
mississippiensis
Empirical
value
(gd-'kPa"1)
Predicted
value
(e-d-EPa-')
Ratio
E/P
1.065
0.020
54.6
0.108
0.020
5.5
0.387
0.091
4.2
* From G. C. Packard et al, 19796. A partial pressure of 1 kPa in the International System of Units is
equal to 7.501 torr.
uid water must also have reduced the conductance of eggs to water vapor, and these
declines in water-vapor conductance probably had the incidental benefit of reducing
transpirational loss of water from exposed
surfaces of eggs to air trapped inside nest
chambers (see Tracy et al., 1978). Among
eggs of contemporary reptiles, conductance to water vapor is related to complexity of the shell layer (G. C. Packard et al,
19796; Lutz et al, 1980). For instance, pliable-shelled eggs of snapping turtles have
conductances that are 55 times higher than
expected for avian eggs of comparable
size, whereas rigid-shelled eggs of softshell
turtles and alligators (Alligator mississippiensis) have conductances that are only 4-6
times higher than expected (Table 5).
Although reptilian eggs have higher
conductances to water vapor than avian
eggs generally, the reptilian eggs do not
necessarily sustain higher rates of transpirational water loss than avian eggs during
the course of natural incubation. Because
the vapor density of air trapped inside subterranean cavities approaches saturation
(G. C. Packard et al, 1979a), the driving
force underlying transpiration from reptilian eggs is extraordinarily low, and the
escape of water vapor from eggs therefore
is minimized. Indeed, when pliable-shelled
eggs of snapping turtles are incubated under hydric conditions simulating those at
the center of natural nests, where eggs are
Conductance of shells to water vapor
supported
by points of contact with other
Evolutionary increases in complexity of
the shell layer leading to reductions in con- eggs and where uptake of liquid water
ductance of eggs of ancestral reptiles to liq- from the substrate is precluded, loss of
360
G. C. PACKARD AND M. J. PACKARD
water vapor leads to declines in mass of
11-18% (G. C. Packard et al., unpublished), which compare favorably with the
decline of 15-18% expected for avian eggs
generally (Rahn and Ar, 1974). Rigidshelled eggs of softshell turtles incubated
under hydric conditions simulating those
at the interior of natural nests decline in
mass by only 4-6% between oviposition
and hatching (G. C. Packard et al., unpublished).
Thus, evolutionary increases in complexity of eggshells probably resulted in
reductions in transpiration of water from
eggs to air inside the nest chambers, thereby conserving water already present in the
yolk and albumen for use by the developing embryo and contributing to the reduced reliance of the embryo upon external sources of water for successful
completion of development.
The avian condition
Although shells of rigid reptilian eggs
are somewhat more porous than shells of
avian eggs generally (Table 5), water-vapor conductance of these reptilian eggs is
not much higher than expected for eggs
of terrestrial birds like the brush turkey
(Alectura lathami), which deposits its eggs in
mounds of loose dirt and dead vegetation
(Seymour and Rahn, 1978)—that is, in
nests similar to those used by reptiles. Furthermore, rigid-shelled eggs of reptiles
probably are functionally cleidoic when incubating in natural nests (G. C. Packard et
al., 1979a), and the cleidoic state usually is
associated with the avian level of organization (Needham, 1931). Thus, rigidshelled eggs of contemporary reptiles approach closely the avian level of organization, and rigid-shelled eggs of ancestral
reptiles can be assumed also to have approached the avian condition.
EVOLUTION OF A COADAPTED COMPLEX
We conclude that the evolution of cleidoic eggs among reptilian ancestors of
birds probably was the result of intense
predation by soil invertebrates and microbes on a highly integrated and coadapted set of characters. Increases in thickness
and complexity of the protective shell layer
led necessarily to reductions in the amount
of water that could be absorbed by incubating eggs from the substrate. Eggs had
therefore to be provisioned with larger
quantities of water at oviposition, thereby
reducing the reliance of embryos upon external sources of water for successful completion of development.4 Reductions in
water-vapor conductance of eggs incidental to adaptive thickening of eggshells led
to reductions in transpirational water loss
during incubation and preadapted eggs
for incubation above ground. The rigidshelled eggs resulting from this evolutionary sequence had acquired an avian level
of organization.
Several factors that are potentially of
great importance have not been treated
here, because pertinent evidence is virtually non-existent. For instance, the few
embryos of contemporary reptiles studied
to date are ureotelic (G. C. Packard et al.,
1977), whereas those of living birds are
uricotelic (Needham, 1931). Thus, the pattern of nitrogen excretion manifested by
developing embryos may have been part
of the coadapted complex undergoing
change during the evolution of avian eggs.
Although urea is relatively non-toxic, it is
quite soluble and occupies "osmotic space."
Consequently, a portion of the water inside reptilian eggs must be used as a solvent for nitrogenous wastes, and is unavailable for use in formation of new
tissue. In contrast, uric acid (or urate salts)
is relatively insoluble, occupies little os4
We note in passing that evolutionary increases in
size of individual eggs attending their provision with
larger quantities of water prior to oviposition must
have led to reductions in potential fecundity of females, owing to the limited volume of eggs that could
be accommodated in the oviducts. This observation
points up the fact that acquisition of a thick, complex
shell layer (and accompanying changes) must have
represented a compromise between conflicting selection pressures, and supports the view that acquisition
of water from outside the eggs can, under certain
circumstances, be of value. Accordingly, it would be
improper to view the evolutionary transition from
naked eggs to shelled eggs as having been driven by
the presumed advantages accruing from increasing
independence of embryos from outside sources of
water, and it would be equally improper to view eggs
with an avian level of organization as being "better"
than eggs with less complex shell layers.
EVOLUTION OF AVIAN EGGS
361
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Ferguson, G. W. and C. H. Bohlen. 1978. DemoACKNOWLEDGMENTS
graphic analysis: A tool for the study of natural
selection of behavioral traits. In N. Greenberg
Our focus on this subject was sharpened
and P. D. MacLean (eds.), Behavior and neurology
considerably in the course of discussions
of lizards, pp. 227-243. U.S. Dept. Health, Eduwith P. R. Sotherland and, especially, T. L.
cation, and Welfare, N.I.M.H., Rockville, MaryTaigen. We thank P. C. H. Pritchard for
land.
supplying the sea turtle eggshells and P. R. Fox, S. F. 1978. Natural selection on behavioral phenotypes of the lizard Uta stansburiana. Ecology
Sotherland for reviewing a draft of this
59:834-847.
paper. The line drawings were executed
Froese, A. D. and G. M. Burghardt. 1974. Food
by K. Jee, and the final typescript was precompetition in captive juvenile snapping turtles,
pared by M. Depperschmidt. Our work
Chelydra serpentina. Anim. Behav. 22:735-740.
has been supported, in part, by a grant Giersberg, H. 1922. Untersuchungen iiber Physiologie und Histologie des Eileiters der Reptilien
from the National Science Foundation
und Vogel; nebst einem Beitrag zur Fasergenese.
(DEB 77-08148).
Z. Wissenschaft. Zool. 120:1-97.
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