Freemartinism in a Captive Herd of Rocky Mountain Bighorn Sheep (Ovis canadensis) Author(s): David E. Kenny, Richard C. Cambre, Michelle W. Frahm, and Thomas D. Bunch Source: Journal of Wildlife Diseases, 28(3):494-498. Published By: Wildlife Disease Association DOI: http://dx.doi.org/10.7589/0090-3558-28.3.494 URL: http://www.bioone.org/doi/full/10.7589/0090-3558-28.3.494

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Journal

Freemartinism

in a Captive

Bighorn

(Ovis

David

Sheep

E. Kenny,’

Gardens, University,

Richard

Herd

C. Cambre,’

Freemartinism

ABSTRACT:

Michelle USA;

of Animal,

in two animals

and Thomas D. Bunch,3 ‘Denver Zoological Zoo, Brownsville, Texas 78520, USA; 3Utah State Dairy and Veterinary Sciences, Logan, Utah 84322, USA Porter

from

Intersex genital

external

genitalia

revealed genitalia. karyotypes mosomes.

a non-patent vagina and internal Both females were chimeric containing XX and XY sex

condition heterosexual

words:

as a yearling.

Intersex,

Rocky Mountain sls, H-Y antigen,

bighorn sheep, M#{252}llerian ducts,

at

the same (Winter and et a!., 1985; McFeely

1980). early

be

Ovis Wolffian

Masculinization in

of

gestation.

associated

is theorized

the

to

an

be

H-Y

genetic Arthur need volve

ducts.

is thought

elaborated

by

to

M#{252}llerian

ducts.

of the become

The

ens, and seminal the influence of primordial tissues androgens

as

the absence ducts (which and anterior

primitive

in

vesicles) androgens. are not the

of H-Y become vagina)

male

normality, upon when

regress.

et in-

in this process at the genetic level could cause a sexual

or ab-

the

1978).

In

Alifakaiotis 1980). Any

severity of it occurs during

in

occur when It happens

fetal

circulation, sac, is shared

there when

is a

through with

a

of cells

established in the other (Dam, 1971). results in a mixed (male

and

female)

bone The popin each

of

the H-Y testicular

antigen, tissue

the and

fepro-

The

male

twin

may

be

less

fertile

and the female twin is sterile (Jubb et a!., 1985; Shanker and Bhatia, 1983; McFeely and Kessly, 1980).

antigen, the M#{252}!lerian the oviducts, uterus, and female genitalia

develop (Jubb et al., 1985; a!., 1976; McFeely et a!., terruption hormonal

ducts defer-

develop under The female stimulated by and

abnormalities

duces androgens thus inhibiting development of M#{252}!lerian ducts and allowing for differentiation of the Wolffian ducts. Freemartin ewes tend to have a more masculine appearance than is characteristic of freemartinism in cattle (Wilkes et a!.,

gonadal

male, the Wolffian the epididymis, vas

which can twinning.

the presence male develops

on

the Y sex chromosome (Jubb et a!., 1985). The fetus initially has a set of undifferentiated gonads and both Wolffian and tissue (which

of

male’s (McFeely and Kessly, 1980; et al., 1982). The anastomosis may to occur early in gestation and inmajor vessels for blood cells from one

ulation

which genes

category

twin making them a chimera and also may transfer the H-Y antigen of the male to the female (McFeely and Kessly, 1980). In

occurs

antigen

and

twin to become marrow of the cellular exchange

1977; Kessly,

fetus

a broad

disorders

genetic female’s the chorioa!lantoic

chro-

fertilization sex normally

Maleness

with

male with

chimera, canaden-

Pfeffer, and

describes

which an animal has the genitalia and/or the secondary sex characteristics of both male and female (Winter and Pfeffer, 1977; Hafez, 1987). Freemartinism is a specific

Necropsy

freemartin,

Gender is determined with the genetic and gonadal being Jubb

pp. 494-498 Association 1992

1992,

Disease

Mountain

of Rocky Mountain bighorn sheep (Ovis canadensis) at the Denver Zoological Gardens (Denver, Colorado, USA) is described. A young ewe had female external genitalia, a masculine appearance, and demonstrated male behavior as she matured. Another ewe with female

Key

28(3),

W. Frahm,2 2Gladys

herd

died

Diseases, © Wildlife

canadensis)

City Park, Denver, Colorado 80205, College of Agriculture, Department

a captive

of Rocky

of Wildlife

Freemartinism ported in domestic in other

species

is most frequently cattle and occasionally including

a!., 1978; McFeely Wilkes et a!. (1978) in

which depends gestation (Jubb

a set

of

triplets

with

genitalia, an enlarged internal reproductive inguina!

et al., 1985). 494

testes,

sheep

and described

epididymes,

(Wilkes

reet

Kessly, 1980). a Dorset ewe female

external

clitoris, and a male tract that included vas

deferentia,

SHORT

and seminal vesicles. or cervix. This animal culine

and

and

male

Williams in a set

when

enlarged uterus,

clitoris, and

ticles. A Rocky ported

section

be

and

(90

and

kg)

(Fig.

genitals

She

also was

casionally the

the

like

herd

the

type

breeding

season ram.

displays,

and (Geist,

to the

in

engaged

in

to

head

12

italia

of

October this

1987,

animal

the

were

ined using manual restraint. typical, except for an enlarged oblong region. showed

masses were present A percutaneous atrophic fibrotic

on histopathologic ized blood samples typing and serum testosterone noassay. herd

levels Samples ram

produced three were transported karyotype

and

ram ocwith

external

gen-

visually

exam-

The vulva clitoris.

another

was Two

inguinal biopsy tissue

Heparinfor karyoto evaluate

utilizing radioim were also submitted

sets

female

who

mufrom has

of twins. All samples on wet ice. For the

5 to 10 metaphase

spreads

formation.

B. Herd

examined

Rocky

by

54 and mosomes

her

also

procedure

dechrowas

contained 2 X chrofemale bighorn sheep

herd

had

ram

normal

and

same

the

were

the

by

presence

This

was

the

second

Berndston

This ointment.

the

mother

ing had

bottle-raising. an enlarged

her

horns

10 mo physical 175

mg

rejected

were of

was

ketamine

a!.

ram were freemartin the normal The high ewe sugtissue.

a female bighorn born on 3 May of three

sets

of

lamb vagina signs of

treated with a topical After the examination the

lamb,

necessitat-

At 5 mo of age she vagina and clitoris developing

age she examination

the

et

twins born to this ewe. The 1-day-old was examined and had an enlarged and clitoris which were showing desiccation. steroidal

The

testosterone following

of testicular

A second case involved who was twin to a male 1989.

control

karyotypes.

for serum animals

described

gested

con-

(1976). The diploid for the freemartin

karyotype (normal The

female

the

Yunis number

karyotype).

big-

male

ram.

following

scribed mosome

Mountain

demonstrating

(1974). The levels for the herd 4.830 ng/ml, for the suspected they were 3.820 ng/ml, and for female they were 0.057 ng/ml. testosterone level of the affected

butting

examination. were taken was collected

male

mount She

in the needle testicular

Captive A. Freemartin

procedure

ram. On

1.

sheep.

1971).

herd

breeding.

horn

radioimmunoassay was run on the

sniffing

attempted

deferred

The

kicking,

ewes

and

but

front

response, other

interested

ram

masculine

a competing

horn of

As she

as the

developed

1). During

ewes

he

by

genitalia.

as large

followed

estrous

pur-

Garden (DZG) (Denver USA) on 20 May 1985 Zoo. She had large horn

(Flehmen)

the

tes-

lamb,

obtained

external

noted

curl

was

grew

behaved

keeper

bighorn

a ewe,

female

she

horns

cervix, ingumnal

FIGURE

matured,

she

per-

female with

rudimentary

Mountain

to

buds

the

was

to the cervix. A right horn. There anastomosis be-

subcutaneous

Denver Zoological Colorado 80205, from a Canadian

if

reported triplets

fetuses in the left horn. The had female external genitalia

no

lip

uterus mas-

days of gestation. The left a male and a female fetus.

The female was closest second male was in the was an arterial umbilical

an

495

behavior.

(1964) of Merino

a caesarian

formed at 146 horn contained

tween fetus

was no appeared

demonstrated

Alexander freemartinism detected

There also

COMMUNICATiONS

was

male

form.

immobilized with a mixture

hydrochloride

still and At for of

(Aveco

496

JOURNAL

OF WILDLIFE

DISEASES,

VOL

28, NO. 3, JULY

1992

cells.

1:’.’

They

were

karyotyped

54XY;

5 54XX,5

54XY,

respectively.

The female premonitory

54XY;

twin signs

as 8 54XX,

2

2 54XX,

8

and

died suddenly of illness at

age. Death was thought ruminal ulcer which lead

14

without mo of

to be due to bacterial

to a co!-

onization and finally a fulminant bacteria! hepatitis. Necropsy also confirmed that the vulva was non-patent and the clitoris markedly was located inguinal

enlarged. The urethral orifice just ventral to the vulva. The masses

examination percutaneous time probably From passed

the testicles through the

abdominal formed bladder. ternal FIGURE tive

2.

tract.

testicle,

Freemartin

a, external and

bighorn female

c, vas

sheep

genitalia;

b,

There female

The

immature

for a chronic lem and at

male

Inc., Fort Dodge, Iowa 50501, USA) 8.75 mg xylazine hydrochloride (MoCorporation, Animal Health Division,

Shawnee,

Kansas

tered

eter

intravenously.

could

advanced

the

vulva.

The

into

surgically

to retention vulvar

A sterile

be

were

lips

long

masses

region.

were

the

phocytes.

lected on wet

in sodium ice from

performed spreads

was

dure analysis chimeras,

of Bunch indicated having

the biopsy

sample

both

lymwas

col-

freemartin Karyo-

by examining following the the

from

and transported her male twin,

from the karyotyping.

et a!.

ob-

inguinal

reactive

heparin this animal,

typing

urine Two

in

blood

sample case for

metaphase

chronic

needle

and a repeat in the first

due

enlarged

perineum.

contained

whole

clitoris

time

the

palpated

masses A

and

at this

A percutaneous of

a few

caused the

cathcenti-

feeding

between

which

around

adminis-

vulva

debu!ked of urine

scalding

USA)

only

meters

one

66201,

(1976). three male

ten proce-

Chromosome bighorns and

were female

earlier

physical

the vasa deferentia inguinal rings into the

was no reproductive

twin

reproductive Co. and bay

on

cavity where seminal vesicles

reproduc-

deferens.

noted

were immature testicles. The biopsy performed at that missed the testicular tissue.

was

debilitating necropsy

they at the

united level

evidence tract

euthanized

and of the

of an (Fig. 3 mo

respiratory had a normal

in2). later

probmale

tract.

The current has been intact

DZG since

bighorn December

sheep 1985.

same ram has been breeding the ewes over this time period. The of the herd ram, first freemartin, of the breeding ewes trace back to The origin of one of the other two

herd The

same 3 lineages and one Canada. breeding

ewes is from the Colorado Rocky Mountains while the second is a descendant of ancestors from the Colorado Rockies and Canada. Offspring from each year are sent to other institutions before the next breeding season and are not bred back to their sire. Twinning is more common in domestic sheep than in cattle; however, freemartins are much more common in cattle. North American wild sheep rarely twin, unlike Asiatic wild sheep (Geist, 1971; Schaller, 1977).

In domestic

92% of heterosexual martins (Marcum,

cattle, approximately twin females 1974). The

are freedifference

in freemartin

rates between

sheep

tle

attributed

the

has

been

to

and

lower

catfre-

SHORT

quency

of major

tomosis

a!.,

in

sheep

1985;

study

twins,

per

ewes

that

brother.

acteristics karyotyping She

had

external

the

very

the freemarborn had not born with a

phenotypic and was

female

hospital

char-

her second a chimera.

genitalia,

testic-

cytogenetics

the

did

not

examine

chiwith

sufficient

phenotypic of

and

the

karyotypic

second

abnor-

freemartin

were

identical to those of the first. She male external genitalia and male genitalia. There or histologically, productive

tween

tract.

Old

The

and

New

The Asiatic wild sheep have a 145 to 155 day tation in North American 180

sheep Asiatic

days.

karyotype

Asiatic

of

showed

that

and

ican

have

sheep

wild

(Geist, is rare

sheep

1971; Schaller, in domestic

the situation Hermaphroditism from were

have

is the

crosses. genitalia

an exploratory

is 170 wild

sheep. and oc-

North

single,

large

Amer-

freemartinism

in

is also

rare event Freemartinism reproductive

same with was reported

lambs

had

with

an

enlarged

celiotomy

female revealed

sheep litters. in

in-

Asiatic wild be similar to

might (0.23 The

North

that The

freemartins/

incidence

of

American

unknown

but

is

wild

probably

a

ACKNOWLEDGMENTS thank

Zoological

Penny

Smith,

Gardens,

zookeeper,

Denver,

Denver

Colorado

for

ex-

cellent observations; The Children’s Hospital Cytogenetics Laboratory, Denver, Colorado for Colorado

State

Endocrine

University,

Laboratory,

Roth

Fort

Collins,

Colorado for testosterone levels; Utah State University, College of Agriculture, Department of Animal, Dairy, and Veterinary Sciences, Logan, Utah for karyotyping; Robert Taylor, Alameda East Veterinary Hospital, Denver, Colorado for surgical assistance; Terry Spraker, Colorado State University,

College

of

Veterinary

Medicine,

Fort

Collins, Colorado for histopathology; Edward Gentz, a former Denver Zoo preceptee and now with Willow Creek Veterinary Clinic, Salt Lake City, Utah for help in researching the case reports. LITERATURE C.,

ALEXANDER,

1976.

Androgen

sheep.

Theriogenology

C. H.,

ARTHUR,

production W.

clitoris tes-

NAOHES,

T.

D.,

in

the

39:

and

sheep

(Ovis).

their

in

PEARSON.

Veterinary

ed.

re-

Bailliere

Tin-

B. W.,

T. M.

AND

of

the

testosterone

NETT.

stallion:

concentra-

Journal

of Reproduc-

115-118.

C.

FOOTE,

Translocations

somes

In

5th

plasma.

W.

H.

AND

cow.

physiology

changes

Fertility

C. FOOTE.

intersexuality

295-327.

Reproductive

tive

W.

AND

of

obstetrics, pp.

of peripheral

136.

CALL,

E., PICKETT,

tion

Ovine

6: 21-24.

D. E.

London,

1964.

1296-1298.

induction

and

Seasonal

1976.

201:

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1974.

ex-

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T. A., J. W.

ALIFAKAIOTIS,

BUNCH,

CITED

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AND

freemartins.

dall,

a ewe and a ram that X Mexican desert lamb

al.,

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BERNDSTON,

wild sheep. in a lamb

This

et

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1982.

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a cross between Agrali-mouflon

bighorn

ges-

European

while

domestic or bore

sheep births).

sheep while

wild

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in domestic heterosexual

sheep

(Bunch

sheep.

domestic

and

triplets

be-

wild

gestation

the they

differences World

were the ancestors of domestic wild sheep commonly twin

casionally

ternal

had feinternal

was no evidence, grossly of an internal female re-

twins in the second case were also chimeric. There are reproductive

and

that 100

497

would be a disadsurvival in species and

of freemartinism is unknown but

Gerber

malities

to

cidence sheep

tissue

twinned

karyotyping;

cells.

The

wild

commonly

We

laboratory

may not have detected they were unfamiliar

or

ovarian

level. at a

and personnel merism because species

of

(Dam, in

tissue and a high testosterone first karyotype was conducted

human

breeds

free-

lambed

of a freemartin, showed she

had

ular The

She

0.23

occurred

inbred lines. The zoo in Canada where tin from the first case was recorded that she had been twin

161

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1980).

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freemartins

In a

Freemartinism for species

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there

100

The

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1991). vantage

(Jubb

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twinning

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McFeely

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