BIOLOGY

OF

46, 39-47

REPRODUCTION

Alligators

Provide

(1992)

Evidence

for the Evolution

BRENT

D.

PALMER,2

of Zoology,

Department

and

of an Archosaurian J.

LOUIS

University

of Florida,

Mode

GUILLE1TE,

Jr.

Gainesville,

Florida

of Oviparity1

32611

ABSTRACT The

female

are

reproductive

layer

calcareous

included

arc

tract

formed

among

the

in

eggs, yet the reproductive

In this

study,

we

examined

that

calcareous

layer.

homologous.

crocodiian

These

uterine

This

mode

with

morphology

of oviparity

that

and

and

uterine

Throughout this the comparative male reproductive

report, the anatomical tract.

term sense

“oviduct” to refer

will be used to the entire

crocodilians

late

ductively

AND

(Griffin,

gravid,

Orange,

gion

were

chemistry, mission

10%

August

Received

May

‘This Water

work

Fish

2Correspondence ical FAX:

and (614)

Biomedical

in part

by a grant

from

the

Game

Electron

and

current Irvine

address Hall,

Brent Ohio

D. Palmer. University,

Department Athens,

OH

may

alligator,

and

membranes

of birds, implicate

and

and may

be

the evolution

immediately

postoviposition,

were

collected

Okeechobee)

and

from

repro-

several

in central

free

and

immediately

lakes

Florida

fixed

microscopy

microscopy

(SEM),

(Per-

for

histo-

and

trans-

(TEM).

washed

in water,

each region or Bouin’s

dehydrated

were fixative.

in graded

and embedded in paraffin sectioned at 7 p.m on a rotary

fixed in Tissues alcohols,

[13]. Specimicrotome,

Microscopy tissue

samples

glutaraldehyde

with

in buffer tetroxide

three for

(15 mm alcohols,

were

minced

0.1

M cacodylate

(1 mm3)

of Zoolog45701-2979.

593-0300.

39

HCI

and buffer

fixed for

times (15 mm each), treated 30 mm, and again washed in each). The specimens treated with 100%

were acetone

de(2

1 h each), and embedded in Spurr’s resin. Thick (1 p.m) were prepared and stained with toluidine

secblue

were cut at 600 A and lead citrate. Microscopic

tissues was performed on a Hitachi HU-11E, or Philips EM-201. Specimens for SEM were cut into 1 cm3 h in 2% glutaraldehyde in 0.1 M cacodylate

Fresh

to LJ.G. Sciences,

birds

electron

buffer three times hydrated in graded

exhibearly

and

and

dissected electron

then

in 2%

Florida

gland

scanning

dye. Thin sections uranyl acetate and

supported

American eggshell

shell

hard-

of soft anatomy.

dyes.

in fe-

6, 1991.

Commission

producing

for a total of 10 slides per tissue specimen, and stained with hematoxylin, eosin, Alcian blue (pH 2.5: for glycosaminoglycans [GAGs]), fast green, orange G, and beibrich scarlet

29, 1991.

was

the

of the

and

and

cleared in xylene, mens were serial

times tions Accepted

oviparous, preservation

Representative tissues from neutral buffered formalin

were

MATERIALS

(Alligator mississippiensis) conditions (vitellogenic,

were

Histology

Specimens alligators reproductive

and

birds

mit #W88063). Within 24 h of capture, the specimens were anesthetized with 20 mg/kg sodium pentobarbital, and the reproductive tracts were surgically removed under sterile conditions. Representative tissues from each oviductal re-

3 h, washed with osmium

Thirty-three iting various

membranes

Phylogenetically,

to poor

archosaur,

quiescent)

For TEM,

METHODS

isthmus

the eggshell

reproduction.

gravid,

Two distinct modes of eggshell formation occur among amniotes. In most reptiles (including chelonians and lepidosaurians) and the monotremes, the uterus produces both the fibrous eggshell membranes and the calcareous layer [1-10]. However, in birds, two spatially distinct regions of the uterus produce separate components of the eggshell (the anterior isthmus forms the eggshell membrane, whereas the posterior shell gland forms the outer calcareous layer [11]). This dichotomy of reproductive anatomy and physiology between birds and other oviparous amniotes may have important implications for our understanding of the evolution of reproductive modes among amniotes. Birds, together with the crocodilians and dinosaurs, make up the archosaurs [12]. This phylogenetic relationship suggests that the other archosaurs also may exhibit the unique “assembly-line” reproductive tract found in birds, with its distinctive mode of eggshell formation. In this study, oviductal functional morphology and ultrastructure were examined during the reproductive cycle of an extant reptilian archosaur, the American alligator, to determine whether it exhibited a “reptilian” or “archosaurian” mode of oviparity.

due

for formation

to the

on dinosaur

INTRODUCTION

dinosaurs

in a reptilian

between

in that

respectively.

gland,

Many

regions

comparable

light

shell

to investigate,

formation

morphology

amniotes

and

dinosaurs.

difficult

eggshell

functional shed

oviparous

isthmus

has separate

ultrastructurally

may

the

has proven

tract

are

of other

uterus:

crocodilians

reproductive regions

that

from

of the

of dinosaurs

of reproductive

similarity

of an archosaurian

system

functional

the

is different regions

along

archosaurs,

shelled

demonstrated

of birds

separate

poststained examination Philips

with of

EM-301,

and fixed for 24 HC1 buffer. Tis-

PALMER and

40

GUILLETI’E

ANTERIOR INFUNDIBULUM

/

/

POSTERIOR INFUNDIBULUM

TUBE

ANTERIOR

POSTERIOR

FIG. ‘I. Gross

sues

were

morphology

dehydrated

114], and sputter-coated was performed on

UTERUS

of a vitellogenic female

in graded with a Hitachi

alcohols,

reproductive

critical

gold. Microscopic S-450.

tract of the American

point

dried

examination

Reproductive

The tor

general

Tract

reproductive

tract

are

characteristics presented

of the

in Figure

seven clearly distinguishable regions along the reproductive tract: anterior infundibulum, fundibulum, tube (tuba uterz’na), utero-tubal terior

uterus,

morphology

posterior

intermedius

ing

alligators

that

thin,

and

vagina

(not

alliga-

1. There

are

the length posterior junction,

of inan-

shown).

The transparent

anterior walls

mnfundibulum and

opens

cells.

is funnel-shaped to the

coelom

with across

The

demarcation

between

tube.

At the

posterior

the

infun-

is indicated by the occurrence of in the tube, which are discernible level by a milky coloration. The

tube is long and convoluted, although that in chelonians. The mucosa of this gitudinally, creating grooves that run the

is tubular, with mucosal folding. although it con-

end

of the

not to the extent of region is folded lonalong the length of

tube

is a short,

narrow

This

to that seen in the crocodile, ro(Guillette, unpublished data), suggestmay serve as a model for crocodilians in

is similar

codylus general.

uterus,

secretory

mississippiensis).

The posterior infundibulum muscular walls and greater true glands in the mucosa,

dibulum and the tube branched acinar glands at the gross morphological

Moiphology

morphological

alligator (Alligator

distal margin. thicker, more There are no tains

RESULTS General

UTERUS

the

FIG. 2. Histology and TEM of the oviductal tube. (A) The mucosal glands of the tube during vitellogenesis are branched acinar and completely fill the lamina propria. IB) The gland cells are characterized by secretory granules of various electron densities. E, luminal epithelium; G, mucosal glands; N, nucleus; S. secretory granules; TL, lumen of tube. Bars: A = 100 p.m; B

=

5 p.m.

ALLIGATOR

REPRODUCTIVE

BIOLOGY

41

42

PALMER

and

GUILLE1TE

REPRODUCTIVE

ALLIGATOR

is visually

distin-

guished by being translucent because it lacks mucosal This is similar to the utero-tubal junction described

region,

the

utero-tubal

glands. in other

oviparous

junction,

amniotes.

rower

than

the

The tube,

which

anterior

and

its

uterine walls

Whereas the tube is flat in cross the anterior uterus is rounded

region

are

(1 cm3) runt proteinaceous these

is nar-

more

muscular.

eggs, consisting of albumen fibers, were observed within

early

gravid

observed glands

(Fig.

extruded

3B).

to those

The transition between the anterior and posterior uterine regions is marked by an increase in the outer diameter, and

Posterior

Uterus

in the pink

fresh

anterior

region

in the

is greater

tissue)

posterior in diameter

change

Each

to a darker

shade posterior

than

vaginal

The following tellogenic and changes throughout

in

pale

uterus.

canal

The the

dometrium is formed into lumen is extremely narrow walls.

from

gray to

uterine region,

tall random and spirals

lumen

and

the

en-

folds. The vaginal through muscular

separately

ultrastructural gravid specimens.

or

of reddish-gray

anterior

opens

cream

into

the

cloaca.

results are based on late-vi(A detailed description of

oviductal histology the reproductive cycle

and morphometrics will be published

The luminal posed of low scribed

for

positively

Tube

the shell idity was

cretory

(Fig.

epithelium columnar 2A). The

of the tube cells: ciliated

ciliated

cells

have

the secretory cells have central, clei. The granules of the secretory Alcian blue dye branched acinar, to

the

surface

slightly

for GAGs. often with (Fig.

apical

nuclei

types se-

whereas

or occasionally, basal, nucells stain intensely with

The glands of the mucosa extensive ducts connecting

2A).

The

The

mucosal

eosmnophilic.

consists of two and microvillous

duct

cells

are

gland

cells

are

mucosal

Anterior In the

gland

cells

metrial necting cuboidal, granules. ical and

numerous

cuboidal

microvilli.

uterus,

stain glands them with

less

luminal

intensely

are branched to the lumen. basal

the

epithelium

with

blue.

tubular, with The endometrial

nuclei

TEM demonstrates electron-dense (Fig.

Alcian

and that 3A).

numerous

these During

The

endo-

short ducts congland cells are eosmnophilic

granules are early gravidity,

sphersmall

FIG. 3. Ultrastructure of the anterior uterus during early gravidity. (A) Electron micrograph of the endometrial glands of the anterior uterus showing electron-dense secretory granules. (B) Scanning electron micrograph showing extrusion of fibers from ducts of the endometrial glands for formation of the eggshell membrane. EF, eggshell fibers; N, nucleus; L, lumen of gland; S, secretory granules. Bars = 10 p.m.

in structure

and

posterior uterus is comcells similar to those de-

However, Alcian

very

blue.

few

The

cells

stained

endometrial

glands

cells have numerous tall microvilli on and extensive interdigitations occur

increases determined

from

the on

are retained in the postewhere eggshell calcificaof the calcareous layer of

early to late by the diameter

graviditv; stage and condition

of grayof the

eggs

from

shells

than

those

the

ends

from

of the the

posterior

uterus

had

thicker

middle.

DISCUSSION A single, production tiles

homogeneous

uterus

of eggshell

[1, 2, 7-10].

of the

In alligators,

The tube

alligator

the

gross

reproductive

and magnum

identified

existence regions, suggests tract

like

hypothesis data. of the 111, 15-17]

trial glands exhibit secretory granules that those of both avian type-A and type-B cells gests that the cells of the alligator tube are

tube functions The translucent (utero-tubal [10,11,15,24].

a more

varied mixture data support the

in albumen transition junction)

dif-

as occurs in that the func-

is more

ultrastructure of birds

rep-

tube of turtles and squamates [1,8-10, 18-22], known to secrete albumen proteins. Cells of the

ized, secreting immunocytochemical

in the

of distinctly

reptiles. This ultrastructural

morphology the

been

in noncrocodilian

uterine of birds,

species than of other by histological and resembles

has

components

ferent anterior and posterior the isthmus and shell gland

consists

layer of ciliated and secretory cells, they are lower and the secretory

similar

were

endometrial

as all shell those

tion

Uterus anterior

using

lateral cell junctions. Eggs uterus for most of gravidity, was apparent. The thickness

avian ported

of a simple columnar as in the tube, although granules

bears

regions.

fibers the

corpora lutea. Most eggs are calcified simultaneously, eggs from a single female had approximately equal thicknesses. However, in the earliest gravid female,

and

or low columnar with basal nuclei. Ultrastructurally, these glands exhibit roughly spherical secretory granules of a wide range of electron densities (Fig. 2B). The apical membrane of the

other

for GAGs

of

membrane.

of the epithelial

are them

cuboidal

are

eggshell

epithelium columnar

(Fig. 4B). These apical membrane,

arately.)

The luminal of tall simple

ducts

by In

of the posterior uterus are branched tubular with cuboidal cells that are not eosinophilic (Fig. 4A). The glandular cells have basal nuclei and lack the extensive distribution of electron-dark secretory granules found in the anterior uterus

their rior tion

sep-

fibers

of the

surrounded this region.

protemnaceous from

These

diameter

(of

specimens,

being

lumen, folds.

a color

section with a wide with tall endometrial

43

BIOLOGY

that

of

is supalligator and which endome-

the is

are similar to [17]. This sugmore general-

of proteins. conclusion

Recent that the

formation in alligators [8, 10, 23]. zone between the tube and uterus occurs in birds and turtles

The anterior uterine region of alligators and ultrastructurally resembles the avian 28] and the homogeneous uterus of other

histochemically isthmus [11, 25reptiles [1,8-10],

44

PALMER

and

UL

GUILLE1TE

REPRODUCTIVE

ALLIGATOR

MODE

OF EGGSHELL

FORMATION

REPRESENTATIVE

45

Eggshell Layers In Single Region The Reproductive

GROUPS

SPATIAL SEPARATION PER EGG EWhell layers formed sequentially on mdividual eggs of a clutch in

BIOLOGY

Formed Of Tract

Eggshell Layers Formed In Separate Regions Of The Reproductive Tract

Birds

separate oviductal regions .41

A

H

,

.41

SPATIAL SEPARATION PER CLUTCH Eggshell layers formed sequentially on an entire clutch in separate oviductal regions

A TEMPORAL

SEPARATION PER CLUTCH Eggshell layers formed sequentially on an entire clutch within a single oviductal region

.41

0.

d

Crocodilians

H

.41

0

E4

0

H

0

0

.41 l ‘41

z

D

c_)

0

C)

.41

o

Ut

Chelonians Squamates Mammals

A NO SEPARATION Eggshell

layers formed simultaneously on an entire clutch within a single oviductal

FIG.

both

Tuatara

region

5.

Increase

of which

in

uterine specialization within oviparous

form

the

fibrous

supports the hypothesis is a uterine specialization. from the the fiber

eggshell

that formation The extrusion

endometrial glands conclusively region of the alligator uterus

amniotes.

membranes.

demonstrates produces the

teinaceous fibers of the eggshell membranes. Unlike the endometrial glands of other reptiles, the alligator’s posterior uterus have cuboidal cells ing

numerous

small,

electron-light

abundant mitochondria, of the avian shell gland, shell

[26, 27].

These

similar which

endometrial

in the release of calcium “plumping” water, which the

albumen

proteins

secretory to the secretes

and crocodilians phology with

modes each

differ

exhibit region

task, such as eggshell cretion [11]. However,

those of contain-

vesicles,

endometrial the calcareous cells

may

that pro-

and

function

eggshell formation and the egg and saturates

reproductive tracts may be homologous,

in ovarian an “assembly performing

membrane birds ovulate

function.

Both

show their birds

line” oviductal moronly one specialized

formation only one

or calcium seegg of a clutch

FIG. 4. Histology and ultrastructure of the posterior uterus (between during early gravidity. (A) The uterine endometrial glands are branched tubular with cuboidal cells. (B) Electron micrograph of the posterior region of the alligator uterus. These cells exhibit few secretory granules (compared to endometrial glands of the anterior uterus), apical microvilli, extensively interdigitated lateral and basal plasma membranes, and abundant mitochondria. E, epithelium; G, endometrial glands; N, nucleus; L, lumen of gland; LI, lateral interdigitations of plasma membranes; M, mitochondna. Bars: A = 100 p.m; B = 5 p.m. eggs)

FIG. 6. Evolutionary tree of amniotic vertebrates (adapted from L#{248}vtrup, 134]) showing evolutionary divergence of oviparous reproductive modes based upon structure and function of the female reproductive tract. 1985

glands egg-

[28, 29].

Although avian and crocodilian great similarities in structure and reproductive

gland

ions for inundates

This

of the membranes of eggshell fibers

at a time ovulate

[30], an

whereas

entire

follicular

growth

stantially

different

on

uterine

share and

and

ovulatory

may

of both

birds

turtles,

represent

are

an that

similar

pattern

function

(monotremes,

most

and and

vergent

evolution.

Factors

confer

a selective

advantage

tracts

morphology such

pothesis

of that

is phylogenetically

such

convergent this

shared based.

am-

Sphenodon)

The

oviductal

and of con-

oviparity

may

an assembly-line

existence

as ovulatory evolution

of alligators

as obligate

for such

type differences,

data

oviparous

because

sembly-line likelihood

These crocodilians

and

However, other groups, such also exhibit obligate oviparity

ological

sub-

that other

of oviduct. monotremes,

of oviduct.

of

therefore

form.

reproductive

in functional

reptiles Control

birds.

squamates,

intermediate

the

are

suggest

birds

other

[31, 32].

alligators

ovarian

It is possible

and

simultaneously

between

and

characteristics

niotes

alligators

clutch

type

as turtles and without an asof major

pattern, and functional

physi-

reduce

support

the

morphology

the hy-

46

and

PALMER

Comparison reptilian

of

taxa,

oviparous

birds,

progression

and

(Fig.

structure leading

reproductive

mammals

5) and

divergence

tween

vertebrate

classes perhaps

REFERENCES

among

(monotremes)

reveals

of reproductive

and function in eggshell to birds occurring within

punctatus),

modes

GUILLETFE

formation, the reptiles,

a

oviparous

with the split and not be-

(Fig. 6). In the tuatara (Sphenodon most anatomically ancient of ex-

the

tant reptiles, both eggshell membranes and calcareous layer are secreted by the uterus simultaneously [7]. Turtle and squamate reproductive tracts exhibit greater specialization with a temporal separation of uterine functions, although both

eggshell

membranes

and

calcium

layer

by the entire, homogeneous uterus [10]. mode and oviductal morphology exhibited [3, 5, 33] resembles of the eggshell are show a divergence tion of formation layers along the hans retained tion, whereas became even

are

Crotaph3’tus

U Jr, Jones

2. Guillene reproductively

histology

and

Trans

Taronga

Zool

1978:

tuatara,

eggs:

of viviparity mammals. of birds

and

model,

crocodilians

which

archosaurs, These productive brates.

may

may

help

elucidate

the

an

BD,

Clearly,

more

work

is required

ical

Influences

in crocodilians

is still unknown

how

and the

eggshell

the egg, where calcium mation, and how these have

important

other

reptiles.

fibers

ions are processes

secreted for are controlled.

phylogenetic

and

Water Service

and

expertise,

Fish Commission

in capturing

of the University

of Florida

I.C,B.R.

Walker

stall

and

assistance

for

and Dr. Franklin

assistance

for

Unit

the

with

of the TEM.

Wesley

Percival

Core

Facility

Medical

and

formation

in eggs

197:147-157. of reptilian modes

oviducts

and

in tetrapod verte-

Dissertation.

morphology

functional fse,nus

of the female

AnsJ Anat

1988; 183(3):200-

and

In: Ferguson

Development Press;

1991:

In: Freeman vol.

their MWJ,

influence

on embryonic

Deeming

in Birds

and

DC (eds.),

Reptiles.

Phys.

Cambridge,

29-46.

BM (ed),

4. London:

The

Academic

AG, Rowe T. Amniote

Physiology

and

Biochemistry

Press; 1983: 379-419.

phylogeny

and

the importance

of fossils.

Tissue

Techniques,

4th

ed. San

Francisco:

WH

Freeman

for

the preservation

for the electron

of three-dimensional

microscope.

Trans

structure

NY Acad

Set 1951;

in

13:130-

genital organs. In: King AS, McLelland J (eds.), Form and 1. London: Academic Press; 1979: 237-360. SE. The characterization and distribution of acidic mucopolvsacchar-

in the

vol.

oviduct

of the

GM, Johnston

infundibulum 1970;

and

domestic

fowl.

HS, Draper

magnum

MI-I,

Res Vet

Sci 1971;

Davidson

of the oviduct

12:225-227.

MF. The

of Ga//us

fine

structure

of the

OJ Exp

domesiscus.

Physiol

55:213-232.

18. Aitken

RNC,

Costa

Solomon

Rican

SE. Observations

green

turtle

on

the

ultrastructure

of the

L.). J Exp

midas

(Chelonia

Mar

oviduct

Biol

Ecol

of 1976;

21:75-90. 19. Bone

V, Granata

20. Bone lizard

of avidin

Laces-ta

by

sicula,

sex

by RNA obtained

synthesis of avidin

hormones.

Gen

synthesis Comp

in the

from

lizard of the

oviduct

Endocrinol

1974;

23:357-

359. reptilien

it

fordata

G. Induction

J Endocrinol 1977; 73:535-536. V, Segal SJ, Koide SS. Induction

21. Giersberg

implica-

his staff Florida

of the Florida to Dr.

Electron

for use of their

Game

U.S. Fish

Henry

for Electron

Center

of shell

biochemistry 1990.

of the

H. tintersuchungen un vogel;

nebst

Uber einem

phvsiologie

beitrag

und

histologie

zur fasergenese.

ZWiss

des

eileiters

Zool

1923;

der 120:1-

97. 22. Weekes

HC.

23.

Placentation

quctyi.

(Hinu/la.) Palmer

BD.

Proc

Albumen

phological

and Linn and

adaptations

other

phenomena

Soc NSW eggshell

1927;

in the

formation

to ecological

Scincid

lizard

Lygosoma

52:499-554. in reptiles:

constraints.

Biol

physiological

and

Reprod

1989;

(eds.),

Physiology

mor-

40(suppl

1)94

141). The

oviduct.

of the

Domestic

RNC.

In:

Hell

Fowl,

DJ, Freeman vol.

3. New

BM York:

Academic

and

Press; 1971:

Bio1237-

1289.

of the

alligators,

activity

31:491-492.

1988(4):105-209.

in Birds,

25. Draper

Hazer

to Alan Woodward

Wales,

AB. Female

16. Solomon ides

ACKNOWLEDGMENTS facilities

ML (ed),

South

secretory

1972; 1988;

proteins

reptiles.

TF. Techniques

Function

chemistry

surgical

of New

135. 15. Gilbert

24. Aitken

to Dr. Fuller

ges-

1979.

17. Wyburn

tions.

indebted

the

of reproductive of Florida;

Embryonic

specimens

(abstract

The authors are greatly

and

GL. Animal

Co;

preparing

around

ecological

and

U Jr. Oviductal

Fowl,

1988;

14. Anderson

eggshell

eggshell These

on Fertil

J Morphol

evolution

University

Kluge

Cladistics and

in reverte-

are wrapped

University

on

Domestic

12. GauthierJ,

the

Particularly,

ft:

SE. Oviduct.

of the

oviducts.

the

on

during

In: Augee

Society

KN, Vos M. Aspects

morphology the

in birds

13. Humason

of other

on how

observations to and

monotremes.

ZDoloejcaI studies

punctatu.s.

for

Guilletie

development

and uterus

divergence in higher

prior

211. 10. Palmer

archosaurian

reproduction

such as dinosaurs. data represent a fundamental system functional morphology

is formed

may

represent

Royal

J Reprod

MB, Goldie

Gainesville,

11. Solomon

such as squamates assembly line

Part 5. Further oviduct

in female

NS\V:

platypus.

Sphenodon

implications

brates.

greater flexibility in adaptation modes,with the eventual rise

in highly derived forms, The specialized oviparous

184:85-

25:1-31.

9 Palmer BD, Guillette U Jr. Histology and reproductive tractof the tortoise G .sspo

to animals with a generalized (multisuch as turtles, squamates, Sphenodon,

have allowed of reproductive

of the

1985;

21:423-443.

of the

Ultrastrucwral

CD. of the

8. Palmer BD. Functional

and mammals, and the other branch evolving a uterus increasingly specialized for eggshell formation, such as cr0codilians and birds. Generalized uterine structure and function may and evolution

morphology

J Morphol

233-253.

MJ, Thompson

of the

1941;

Mosman,

epithelium

7. Packard

ovulaformation ovulation,

physiology),

1989;

Part I. The histology of the oviduct

1933;

activity

FN. Reproduction

RL, Shore)’

oviduct

with

(and

placental

aeneus.

of the Monotremasa.

secretory

Soc Lond

Biology. Zoo;

6. Hughes

6) of female

anatomy

in the

obsoletus.

and

S elcpcnis

Soc Lond

Zool

the

RL, Carrick

Monotrenie

re(Fig.

reproductive

oviductal

species,

of the Monotremata.

Trans

UK: Cambridge

leading uterus,

lizard

development

gestation.

tation.

so that each egg of a clutch is shelled individually. The assembly line morphology of the archosaurian productive tract may represent a functional divergence one branch functional)

RE. Ovarian,

bimodal

CJ. The

during

5. Hughes

from this pattern in the spatial separaof membranous and calcareous eggshell length of the reproductive tract. Crocodi-

and egg shelling J Morphol

Eumeces

98. 3. Hill

the

in that all layers The archosaurs

morphology

and

colla,-is

201:145-159.

produced

the ancestral mode of simultaneous in birds the process of eggshell more specialized with sequential

lizards

4. Hill CJ. The development

The reproductive by monotremes

those of these reptiles deposited in the uterus.

1. GuilletteU Jr,Fox SL, Palmer BD. Oviductal

tract

Aldrich

Microscopy, Microscopy

and

Fresh

and Wildlife and and

the staff to Nola

Laboratory

MI-I,

Davidson

fibrous

membrane

mesticus.

OJ Exp

26. Solomon 1975;

Physiol

SE. Studies

region 1972;

on the

GM.

Johnston

of the

isthmus

HS. The

fine

of the

oviduct

of the

structure of Gal/us

do-

Brit

Set

57:297-310.

isthmus

region

of the

domestic

fowl.

Poult

16:255-258.

27. Wyburn shell

MF, Wyburn forming

GM. Johnston forming

domesticus.

region

HS, of the

OJ Exp Phvsiol

Draper

MB,

Davidson

oviduct

and

1973;

58:143-151.

MF. The

the development

ultrastructure of the shell

of the of Gal/us

ALLIGATOR

28.

Breen

(shell 29. Tract’ eggs,

PC, de Brun

PPH.

The

fine

structure

gland) of the chicken. J Morphol CR, Snell HL. Interrelations among embryos,

and

hatchlings.

Am

Zool

of the

secretory

1969: 128:35-66. water and energy 1985:

cells relations

REPRODUCTIVE

of the

uterus

of reptilian

25:999-1008.

Gilbert AB. Female genital organs. In: King AS, McLelland J (eds.), Form and Function in Birds. vol. 1. London. Academic Press, 1979: 237-360. 31. Jones RE, Fitzgerald KT, Duvall D, Banker D. On the mechanisms of alternating and

simultaneous

ovulation

in lizards,

Herpetologica

1979;

32.

Lance

33.

1018. Hughes tremes

30.

35(2):132-139.

47

BIOLOGY

VA. Reproductive RU. Egg and

cycle

membranes

marsupials.

of the American and

oyarian

In: Reproduction

Academy of Science: 1977281-291 34. L#{248}vtrupS. On the classification of the 470

Am Zool

alligator. function

during

and Evolution. taxon

Tetrapoda.

1989;

29(3 ):999-

pregnancy

Canberra Svsi Zool

in mono-

City:

Australian

1985:

34:463-