Burns Et Al. 2011. Male Reproductive Traits and Their Relationship To Reproductive Traits in Their

Review Article
Male Reproductive Traits and Their Relationship to Reproductive Traits in Their

Female Progeny: A Systematic Review
BM Burns
1
, C Gazzola
2
, RG Holroyd
2
, J Crisp
3
and MR McGowan
3
1
The University of Queensland, Centre for Animal Science, Queensland Alliance for Agriculture and Food Innovation, Rockhampton, Qld, Australia;
2
Department of Employment, Economic Development and Innovation, Rockhampton, Qld, Australia;
3
The University of Queensland, School of
Veterinary Science, Gatton, Qld, Australia
Contents
The overall objective of one of the major research programs in
the Co-operative Research Centre (CRC) for Beef Genetic
Technologies is to Improve female reproductive performance
in tropical, northern Australian beef cattle herds. To address
this overall objective, a quantitative genetics project focused
on investigation of male reproductive traits was designed and
linked to three female reproductionfocussed projects, (i)
discovery of genes associated with post-partum re-conception
and age at puberty; (ii) expression of genes associated with
post-partum re-conception; and (iii) early predictors of lifetime
female reproductive performance. During the initial planning
of this male reproductive traits project, the CRC Scientic
Review Committee recommended that the research team
investigate and evaluate potentially new, early-life (i.e able
to be measured before 2 years of age) predictors of both male
and female reproductive performance. To address this recom-
mendation, the following was carried out: (i) criteria for
selection of traditional and candidate traits were established;
(ii) methodology for tabulation of potential traits phenotypes
that dene male and female reproductive function was
developed; and (iii) a systematic scientic review of early-life
predictors of male and female fertility was prepared. This
review concluded that although factors that might be useful in
predicting male reproductive performance have been studied
for many years, there was relatively little useful information
available to meet the objectives of this review. It was also
concluded that the direction of future research should be
guided not only by previous research which was scarce, but
also by speculative hypotheses arising from an understanding
of the physiological, endocrinological and genetic processes
active in reproduction. A small number of new traits were
recommended in addition to traditional sperm morphology,
sexual behaviour, anatomical structure and growth traits.
Potential additional traits include measurement of gonadotro-
phin-releasing hormone-stimulated luteinizing hormone
(GnRH-stimulated LH); inhibin; several seminal plasma pro-
teins (osteopontin, spermadhesin and seminal plasma proteins
BSP30 and phospholipase A
2
could be used in an index); 11b-
hydroxysteriod dehydrogenase; and leptin. In addition, the
potential also exists to screen animals for a number of genetic
markers associated with age of puberty, follicular recruitment
and ovulation rate and genes associated with bovine seminal
plasma protein and testosterone production. Insulin-like
growth factor-1 (IGF-1) measurements are included because
of their association with growth parameters, and an additional
analysis demonstrated associations with male and female
reproductive traits. Some of these factors have been previously
evaluated in small numbers of animals of various species under
intensive management conditions. Therefore, there is a need to
evaluate these factors in much larger numbers of beef cattle
grazing semi-extensive tropical production systems in northern
Australia to determine their value in improving beef cattle
enterprise protability through improved herd fertility.
Introduction
A major limitation to northern Australian beef cattle
herds is that direct selection for cow fertility can only
be applied to females, usually at low intensities, and
relatively late in life when the cows have one or two
calving records (Mackinnon et al. 1989). This problem
could be overcome if herd traits in males were
identied that were genetically correlated to female
fertility traits, and these male traits were able to be
measured early in life (Mackinnon et al. 1989). In
addition, Walkley and Smith (1980) reported in sheep
that if a trait could be identied in young males,
which was correlated with the reproductive perfor-
mance of adult females, the potential would exist to
double the selection intensity, and therefore the rate of
genetic change, by selecting in both males and
females.
Land (1973) proposed that because the hormonal
control of reproductive function is similar in the two
sexes, one might expect that male and female reproduc-
tive traits would be closely correlated genetically.
Darwash et al. (1999) have also reported that there is
a growing body of evidence suggesting that the majority
of endocrine factors associated with reproduction in
dairy cattle are a result of dierential gene expression in
the hypothalamus, pituitary, ovary and uterus.
In conclusion, it may be possible to identify early-life
predictors of fertility both phenotypically (a bulls
fertility as reected by improved calf output) and
genetically (the fertility of a bulls female and male
progeny). To further investigate the potential use of this
approach to improve the reproductive performance of
beef cattle, in particular tropically adapted genotypes, a
systematic review of the published literature on male
reproductive traits and their relationship to reproductive
traits in their female progeny was conducted.
Objective of the Review
To identify male traits potentially genetically correlated
with female fertility traits, with particular emphasis on
identifying traits which could be assessed in pre-pubertal
bulls.
Reprod Dom Anim 46, 534553 (2011); doi: 10.1111/j.1439-0531.2011.01748.x
ISSN 0936-6768
The State of Queensland (through the Department of Employment, Economic Development and Innovation) 2011
Materials and Methods
The systematic review was conducted as follows:
1. Publications were reviewed to examine the rela-
tionship between various bovine male traits and the
fertility of the male and or the fertility of his male or
female ospring. Non-bovine mammalian publica-
tions were also examined.
2. The search was restricted to testicular, seminal and
hormonal traits only as mating behaviour can only be
measured reliably in sexually mature bulls.
3. Those publications that quantied the relationship
between measured traits and fertility and provided
estimates of the heritability of traits and the genetic
correlations between male and female traits were
examined in detail.
4. Traits that, from a developmental (embryological)
or physiological (endocrinological) point of view,
have the potential to predict both male and female
reproductive function were considered.
The selection criteria for candidate early-life predic-
tors of male fertility and fertility of male and female
ospring were as follows:
1. Male traits that were moderately heritable and
moderately genetically correlated with female traits
were given an initial high ranking.
2. Consideration was given to potential novel traits
whose case for selection could be based on the
theoretical potential of the trait to predict fertility
based on whatever direct or derived knowledge was
available.
3. Traits were grouped according to those that could
be measured in the pre-pubertal bull and those that
could only be measured after the bull reached
puberty. Within each of these categories, traits were
further grouped according to their capacity to assess
one of the followings:
(i) Testicular development;
(ii) Endocrine control of testis function;
(iii) Spermatogenesis; and
(iv) Fertilizing potential of sperm.
4. Traits that require sampling methods that are
highly invasive, require multiple samples to be
collected and are very expensive or detrimental to
the future fertility of the animal were given an initial
low ranking.
Results and Discussion
The ndings from this systematic review have been
summarized to four tables (Tables 14) under the
following headings:
1. Male reproductive traits and their relationship to
other measures of reproductive function in the male.
2. Male phenotypic traits and their correlated traits in
female progeny.
3. Heritability of male traits and correlated female
progeny traits.
4. Genetic markers of male reproductive traits with
eects on female progeny.
Age-corrected scrotal circumference was consistently
reported to be a useful method of assessing reproductive
function in bulls (Table 1) because of the favourable
relationship with a number of sperm traits (Brinks et al.
1978) and fertility (Mackinnon et al. 1990b). Pre-
pubertal basal serum follicle-stimulating hormone
(FSH) concentration was identied as a potential
candidate trait because of its role in the endocrine
control of testicular function and its moderate correla-
tion with Sertoli cell number (Moura and Erickson
1997) (Table 1). The reported moderate correlation
between pre-pubertal basal serum luteinizing hormone
(LH) concentration and age of puberty also suggested
that this trait may be a useful early-life predictor of
fertility (Aravindakshan et al. 2000) (Table 1). How-
ever, these measurements require multiple sampling
under commercial industry conditions.
In contrast, GnRH-stimulated release of LH in pre-
pubertal bulls reported by Moura and Erickson (1997)
and Bagu et al. (2006) may be a practical alternative
(Table 1). This test is simpler than multiple samplings as
it requires an initial pre-injection blood sample, followed
by an injection of GnRH analogue, and a subsequent
single 0.5 to 1 hourly blood sample. However, there are
only a small number of publications describing the use
of this test, and except for one study in bulls from
1626 months of age (Perry et al. 1990a), most studies
have only monitored the bulls to yearling age (Moura
and Erickson 1997; Bagu et al. 2006) (Table 1). Perry
et al. (1990a) reported that the best fertility indices,
which included GnRH-stimulated LH, were those
assessed at 11, 8, 6 and 2 months prior to mating and
were collectively signicantly correlated with pregnancy
rate (P < 0.01). However, Perry et al. (1990a) also
reported that these tests carried out on the bulls
immediately prior to and immediately post-mating did
not result in strong correlations with pregnancy rates. In
addition, in two separate studies using four Hereford-
Shorthorn bulls and three Zebu British cross-bred
bulls (bulls aged 1729 months were individually joined
with groups of 1930 cows), respectively, Post et al.
(1987) reported that the bulls with the highest peak
plasma testosterone concentrations 22.5 h after intra-
muscular injection with GnRH achieved the highest
overall fertility [capable cows pregnant; highest libido
(oestrous cows mated) and fertilizing ability (mounted
cows pregnant)]. Further, the rankings of the Bos indicus
bulls for both reproductive performance and testoster-
one response to GnRH were repeatable when measured
at two and four years of age (Post et al. 1987).
Therefore, these studies suggest that it would be useful
to conduct a study of GnRH-stimulated release of LH in
pre-pubertal bulls at around 23 months of age and then
evaluate these animals through puberty up to 2 years of
age. The GnRH-stimulated LH relationship with testes
function, in terms of age at puberty and age at which a
normal spermiogram is recorded, could be investigated
given the experimental design of the CRC Male
indicator traits to improve female reproductive perfor-
mance Project. However, it is acknowledged that
conducting the GnRH response test is reasonably labour
intensive.
Male and Female Reproductive Traits 535
T
a
b
l
e
1
.
M
a
l
e
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
a
n
d
t
h
e
i
r
r
e
l
a
t
i
o
n
s
h
i
p
w
i
t
h
o
t
h
e
r
m
e
a
s
u
r
e
s
o
f
r
e
p
r
o
d
u
c
t
i
v
e
f
u
n
c
t
i
o
n
i
n
t
h
e
m
a
l
e
(
a
)
P
r
e
-
p
u
b
e
r
t
a
l
t
r
a
i
t
s
;
(
b
)
p
o
s
t
-
p
u
b
e
r
t
a
l
t
r
a
i
t
s
(
>
2
y
e
a
r
s
o
l
d
)
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
M
a
l
e
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
(
a
)
P
r
e
-
p
u
b
e
r
t
a
l
t
r
a
i
t
s
C
o
r
r
e
c
t
e
d
S
C
(
S
C
A
g
e
)
B
r
i
n
k
s
e
t
a
l
.
(
1
9
7
8
)
C
a
t
t
l
e
;
H
,
A
1
2
m
o
l
M
o
t
i
l
i
t
y
%
%
p
r
i
m
a
r
y
a
b
n
o
r
m
a
l
i
t
y
%
s
e
c
o
n
d
a
r
y
a
b
n
o
r
m
a
l
i
t
y
%
n
o
r
m
a
l
0
.
2
5
)
0
.
5
1
)
0
.
4
2
0
.
5
8
S
c
r
o
t
a
l
c
i
r
c
u
m
f
e
r
e
n
c
e
f
a
v
o
u
r
a
b
l
y
c
o
r
r
e
l
a
t
e
d
w
i
t
h
a
l
l
s
e
m
e
n
t
r
a
i
t
s
e
v
a
l
u
a
t
e
d
.
n
=
2
8
7
M
a
c
k
i
n
n
o
n
e
t
a
l
.
(
1
9
9
0
b
)
C
a
t
t
l
e
;
D
r
9
m
o
1
2
m
o
1
8
m
o
l
D
i
e
r
e
n
c
e
i
n
S
C
b
e
t
w
e
e
n
h
i
g
h
-
a
n
d
l
o
w
-
f
e
r
t
i
l
i
t
y
l
i
n
e
s
(
E
B
V
f
o
r
P
R
)
H
i
g
h
L
o
w
5
.
8
m
m
H
i
g
h
L
o
w
9
.
6
m
m
H
i
g
h
L
o
w
1
6
.
0
m
m
n
=
1
1
1
F
o
l
l
i
c
l
e
-
s
t
i
m
u
l
a
t
i
n
g
h
o
r
m
o
n
e
(
b
a
s
a
l
F
S
H
)
M
o
u
r
a
a
n
d
E
r
i
c
k
s
o
n
(
1
9
9
7
)
C
a
t
t
l
e
;
A
2
1
2
m
o
2
3
m
o
8
1
2
m
o
9
1
2
m
o
s
m
Y
e
a
r
l
i
n
g
S
C
S
e
r
t
o
l
i
c
e
l
l
n
u
m
b
e
r
R
S
)
0
.
5
3
t
o
)
0
.
7
4
)
0
.
5
1
t
o
)
0
.
5
4
)
0
.
4
7
t
o
)
0
.
5
3
)
0
.
5
6
t
o
)
0
.
6
4
n
=
2
4
R
S
(
r
o
u
n
d
s
p
e
r
m
a
t
i
d
s
p
e
r
S
e
r
t
o
l
i
c
e
l
l
)
A
r
a
v
i
n
d
a
k
s
h
a
n
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
H
C
1
1
0
m
o
s
m
A
g
e
p
u
b
e
r
t
y
n
s
n
=
2
0
B
a
s
e
d
o
n
2
s
m
a
l
l
g
r
o
u
p
s
s
e
l
e
c
t
e
d
f
o
r
a
g
e
p
u
b
e
r
t
y
L
u
t
e
i
n
i
z
i
n
g
h
o
r
m
o
n
e
(
m
e
a
n
L
H
)
M
o
u
r
a
a
n
d
E
r
i
c
k
s
o
n
(
1
9
9
7
)
C
a
t
t
l
e
;
A
2
1
2
m
o
s
m
Y
e
a
r
l
i
n
g
S
C
n
s
n
=
2
4
A
r
a
v
i
n
d
a
k
s
h
a
n
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
H
C
1
m
o
2
.
5
m
o
9
m
o
s
m
A
g
e
p
u
b
e
r
t
y
)
0
.
5
6
)
0
.
5
1
)
0
.
7
6
n
=
2
0
B
a
s
e
d
o
n
2
s
m
a
l
l
g
r
o
u
p
s
s
e
l
e
c
t
e
d
f
o
r
a
g
e
p
u
b
e
r
t
y
L
u
t
e
i
n
i
z
i
n
g
h
o
r
m
o
n
e
(
p
u
l
s
e
f
r
e
q
u
e
n
c
y
L
H
)
A
r
a
v
i
n
d
a
k
s
h
a
n
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
H
C
2
.
5
m
o
5
m
o
s
m
A
g
e
p
u
b
e
r
t
y
)
0
.
6
7
)
0
.
5
1
n
=
2
0
B
a
s
e
d
o
n
2
s
m
a
l
l
g
r
o
u
p
s
s
e
l
e
c
t
e
d
f
o
r
a
g
e
p
u
b
e
r
t
y
T
e
s
t
o
s
t
e
r
o
n
e
M
o
u
r
a
a
n
d
E
r
i
c
k
s
o
n
(
1
9
9
7
)
C
a
t
t
l
e
;
A
2
1
2
m
o
s
m
Y
e
a
r
l
i
n
g
S
C
n
s
n
=
2
4
A
r
a
v
i
n
d
a
k
s
h
a
n
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
H
C
1
1
0
m
o
s
m
A
g
e
p
u
b
e
r
t
y
n
s
n
=
2
0
B
a
s
e
d
o
n
2
s
m
a
l
l
g
r
o
u
p
s
s
e
l
e
c
t
e
d
f
o
r
a
g
e
p
u
b
e
r
t
y
G
o
n
a
d
o
t
r
o
p
h
i
n
-
r
e
l
e
a
s
i
n
g
h
o
r
m
o
n
e
s
t
i
m
u
l
a
t
e
d
F
S
H
(
G
n
R
H
-
s
t
i
m
u
l
a
t
e
d
F
S
H
)
M
o
u
r
a
a
n
d
E
r
i
c
k
s
o
n
(
1
9
9
7
)
C
a
t
t
l
e
;
A
2
1
2
m
o
s
m
Y
e
a
r
l
i
n
g
S
C
n
s
t
o
)
0
.
7
1
n
=
2
4
C
o
u
l
d
b
e
u
s
e
f
u
l
a
t
s
o
m
e
a
g
e
s
,
b
u
t
d
a
t
a
n
o
t
g
i
v
e
n
A
r
a
v
i
n
d
a
k
s
h
a
n
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
H
C
1
1
0
m
o
s
m
A
g
e
p
u
b
e
r
t
y
n
s
n
=
2
0
B
a
s
e
d
o
n
2
s
m
a
l
l
g
r
o
u
p
s
s
e
l
e
c
t
e
d
f
o
r
a
g
e
p
u
b
e
r
t
y
G
n
R
H
-
s
t
i
m
u
l
a
t
e
d
t
e
s
t
o
s
t
e
r
o
n
e
M
o
u
r
a
a
n
d
E
r
i
c
k
s
o
n
(
1
9
9
7
)
C
a
t
t
l
e
;
A
3
m
o
2
1
2
m
o
s
m
Y
e
a
r
l
i
n
g
S
C
T
e
s
t
o
s
t
e
r
o
n
e
0
.
4
8
0
.
4
8
t
o
0
.
5
6
n
=
2
4
G
n
R
H
-
s
t
i
m
u
l
a
t
e
d
L
H
H
a
l
e
y
e
t
a
l
.
(
1
9
8
9
)
S
h
e
e
p
2
.
5
5
m
o
s
m
S
e
l
e
c
t
i
o
n
l
i
n
e
s
G
n
R
H
-
s
t
i
m
F
S
H
S
C
a
t
s
a
m
e
a
g
e
0
.
4
0
0
.
1
4
P
e
r
r
y
e
t
a
l
.
(
1
9
9
0
a
)
C
a
t
t
l
e
1
6
m
o
1
8
m
o
2
0
m
o
2
4
m
o
2
6
m
o
s
m
P
R
0
.
7
1
0
.
7
6
0
.
7
3
0
.
6
6
0
.
4
5
S
e
v
e
r
a
l
b
r
e
e
d
s
,
g
o
o
d
i
f
h
o
l
d
s
u
p
p
r
e
-
p
u
b
e
r
t
y
.
I
n
c
o
n
v
e
n
i
e
n
t
m
e
a
s
u
r
e
m
e
n
t
p
r
o
c
e
d
u
r
e
M
o
u
r
a
a
n
d
E
r
i
c
k
s
o
n
(
1
9
9
7
)
C
a
t
t
l
e
;
A
2
1
2
m
o
s
m
B
a
s
a
l
L
H
B
a
s
a
l
F
S
H
G
n
R
H
s
t
i
m
F
S
H
a
G
n
R
H
s
t
i
m
F
S
H
b
0
.
6
5
0
.
4
8
0
.
6
9
0
.
7
5
a
a
n
d
b
D
i
e
r
e
n
t
t
i
m
e
s
a
f
t
e
r
s
t
i
m
u
l
a
t
i
o
n
536 BM Burns, C Gazzola, RG Holroyd, J Crisp and MR McGowan
T
a
b
l
e
1
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
M
a
l
e
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
A
r
a
v
i
n
d
a
k
s
h
a
n
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
H
C
1
1
0
m
o
s
m
A
g
e
p
u
b
e
r
t
y
n
s
n
=
2
0
B
a
s
e
d
o
n
2
s
m
a
l
l
g
r
o
u
p
s
s
e
l
e
c
t
e
d
f
o
r
a
g
e
p
u
b
e
r
t
y
.
S
o
m
e
s
t
a
t
i
s
t
i
c
s
o
f
c
o
n
c
e
r
n
w
i
t
h
s
u
b
-
g
r
o
u
p
s
B
a
g
u
e
t
a
l
.
(
2
0
0
6
)
C
a
t
t
l
e
,
H
C
1
5
m
o
s
m
P
r
e
d
i
c
t
e
a
r
l
y
p
u
b
e
r
t
y
(
s
i
g
n
i
c
a
n
t
p
<
0
.
0
5
e
e
c
t
)
L
H
r
e
s
p
o
n
s
e
s
t
o
l
u
t
e
i
n
i
z
i
n
g
h
o
r
m
o
n
e
-
r
e
l
e
a
s
i
n
g
h
o
r
m
o
n
e
(
L
H
R
H
o
r
G
n
R
H
)
i
n
1
-
t
o
5
-
m
o
-
o
l
d
c
a
l
v
e
s
c
o
u
l
d
b
e
u
s
e
d
t
o
s
e
l
e
c
t
e
a
r
l
y
m
a
t
u
r
i
n
g
b
u
l
l
s
I
n
h
i
b
i
n
M
i
y
a
m
o
t
o
e
t
a
l
.
(
1
9
8
9
)
C
a
t
t
l
e
;
J
a
p
<
8
m
o
s
m
L
e
v
e
l
h
i
g
h
u
p
t
o
4
m
o
C
o
r
r
.
F
S
H
<
4
m
o
C
o
r
r
.
t
e
s
t
o
s
t
.
<
4
m
o
0
.
6
9
)
0
.
5
8
S
e
r
u
m
i
n
h
i
b
i
n
v
a
l
i
d
m
e
a
s
u
r
e
o
f
i
n
h
i
b
i
n
p
r
o
d
u
c
t
i
o
n
a
t
y
o
u
n
g
a
g
e
.
F
S
H
a
n
d
i
n
h
i
b
i
n
n
o
t
a
n
t
a
g
o
n
i
s
t
i
c
a
t
y
o
u
n
g
a
g
e
M
a
c
D
o
n
a
l
d
e
t
a
l
.
(
1
9
9
1
)
C
a
t
t
l
e
;
H
o
1
9
m
o
s
m
I
n
h
i
b
i
n
p
e
a
k
s
2
3
m
o
L
e
j
e
u
n
e
e
t
a
l
.
(
1
9
9
7
)
P
i
g
1
m
o
c
e
l
l
s
B
a
s
a
l
t
e
s
t
o
s
t
e
r
o
n
e
n
o
e
e
c
t
h
C
G
-
s
t
i
m
t
e
s
t
o
s
1
4
0
%
L
H
b
i
n
d
i
n
g
3
7
%
L
H
R
m
R
N
A
1
7
5
%
1
7
a
H
a
s
e
m
R
N
A
5
0
0
%
I
n
v
i
t
r
o
:
i
m
m
a
t
u
r
e
(
3
w
e
e
k
)
p
i
g
L
e
y
d
i
g
c
e
l
l
s
.
A
c
t
i
v
i
n
a
l
s
o
t
e
s
t
e
d
M
a
t
s
u
z
a
k
i
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
H
o
2
1
2
m
o
s
m
L
e
v
e
l
s
h
i
g
h
t
o
7
m
o
t
h
e
n
L
o
w
S
t
u
d
y
p
r
e
s
e
n
t
s
c
h
a
n
g
i
n
g
l
e
v
e
l
s
o
f
i
n
h
i
b
i
n
,
F
S
H
,
L
H
a
n
d
t
e
s
t
o
s
t
e
r
o
n
e
f
r
o
m
2
.
5
t
o
1
0
m
o
K
a
n
e
k
o
e
t
a
l
.
(
2
0
0
1
)
C
a
t
t
l
e
;
H
o
0
3
m
o
s
m
I
n
h
i
b
i
n
r
i
s
e
s
t
o
3
m
o
I
n
h
i
b
i
n
p
a
r
a
l
l
e
l
s
F
S
H
I
n
h
i
b
i
n
a
n
d
F
S
H
n
o
t
a
n
t
a
g
o
n
i
s
t
i
c
a
t
y
o
u
n
g
a
g
e
s
W
h
e
a
t
o
n
a
n
d
G
o
d
f
r
e
y
(
2
0
0
3
)
S
h
e
e
p
P
r
e
-
p
u
b
e
r
t
a
l
s
m
A
n
t
i
-
i
n
h
i
b
i
n
i
m
m
u
n
e
a
g
e
p
u
b
e
r
t
y
F
S
H
n
o
c
h
a
n
g
e
L
H
L
H
p
u
l
s
e
n
o
c
h
a
n
g
e
t
e
s
t
o
s
t
e
r
o
n
e
S
C
n
o
e
e
c
t
D
e
m
o
n
s
t
r
a
t
e
s
t
h
e
d
i
e
r
e
n
t
e
e
c
t
s
o
f
i
n
h
i
b
i
n
b
e
f
o
r
e
a
n
d
a
f
t
e
r
p
u
b
e
r
t
y
i
.
e
.
b
e
f
o
r
e
p
u
b
e
r
t
y
i
t
i
n
c
r
e
a
s
e
s
f
e
r
t
i
l
i
t
y
-
a
s
s
o
c
i
a
t
e
d
c
h
a
r
a
c
t
e
r
i
s
t
i
c
s
K
a
n
e
k
o
e
t
a
l
.
(
2
0
0
3
)
C
a
t
t
l
e
;
J
a
p
1
1
5
m
o
s
m
C
h
a
n
g
e
i
n
m
o
l
e
c
u
l
a
r
s
p
e
c
i
e
s
a
t
p
u
b
e
r
t
y
f
o
r
m
4
7
D
a
t
o
3
0
k
D
a
b
o
t
h
i
n
h
i
b
i
n
A
&
B
.
I
n
h
i
b
i
n
p
r
o
d
u
c
e
d
e
x
c
l
u
s
i
v
e
l
y
b
y
S
e
r
t
o
l
i
c
e
l
l
s
T
a
b
l
e
1
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
M
a
l
e
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
S
h
a
r
p
e
e
t
a
l
.
(
2
0
0
3
)
R
e
v
i
e
w
V
a
r
i
o
u
s
s
p
e
c
i
e
s
R
o
l
e
o
f
p
r
e
-
p
u
b
e
r
t
a
l
S
e
r
t
o
l
i
c
e
l
l
d
e
v
e
l
o
p
m
e
n
t
a
n
d
u
s
e
o
f
i
n
h
i
b
i
n
t
o
p
r
e
d
i
c
t
S
e
r
t
o
l
i
c
e
l
l
n
u
m
b
e
r
I
G
F
-
1
Y
i
l
m
a
z
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
;
A
5
6
m
o
6
8
m
o
s
m
A
d
u
l
t
S
C
M
o
t
i
l
i
t
y
A
d
u
l
t
S
C
M
o
t
i
l
i
t
y
0
.
2
4
0
.
1
4
0
.
2
3
0
.
3
7
0
.
2
6
0
.
0
6
0
.
5
6
0
.
2
8
0
.
1
6
0
.
0
7
0
.
1
3
0
.
0
4
S
e
l
e
c
t
i
o
n
o
f
h
i
g
h
a
n
d
l
o
w
l
i
n
e
s
s
t
a
r
t
e
d
1
9
8
9
1
9
9
0
a
n
d
i
n
b
r
e
e
d
i
n
g
c
o
n
t
i
n
u
e
d
w
i
t
h
n
=
8
b
u
l
l
s
p
e
r
y
e
a
r
a
n
d
n
=
1
0
0
c
o
w
s
p
e
r
y
e
a
r
T
h
o
m
a
s
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
;
A
,
B
r
,
B
6
8
m
o
s
m
S
C
a
t
s
a
m
e
a
g
e
0
.
7
3
n
=
2
1
L
e
p
t
i
n
T
h
o
m
a
s
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
;
A
,
B
r
,
B
6
8
m
o
s
m
S
C
a
t
s
a
m
e
a
g
e
0
.
6
7
n
=
2
1
(
b
)
P
o
s
t
-
p
u
b
e
r
t
a
l
t
r
a
i
t
s
(
>
2
y
e
a
r
o
l
d
)
T
e
s
t
i
c
u
l
a
r
M
e
a
s
u
r
e
m
e
n
t
s
C
o
r
r
e
c
t
e
d
S
C
(
S
C
A
g
e
)
B
a
m
u
a
l
i
m
e
t
a
l
.
(
1
9
8
4
)
C
a
t
t
l
e
;
D
r
2
y
e
a
r
7
y
e
a
r
l
S
a
m
e
y
e
a
r
P
R
L
i
f
e
t
i
m
e
P
R
n
s
n
s
P
o
s
t
-
p
u
b
e
r
t
a
l
.
C
o
r
r
e
c
t
e
d
S
C
(
S
C
A
g
e
)
H
a
h
n
e
t
a
l
.
(
1
9
6
9
a
)
C
a
t
t
l
e
;
d
a
i
r
y
b
u
l
l
s
Y
o
u
n
g
d
a
i
r
y
b
u
l
l
s
l
S
p
e
r
m
o
u
t
p
u
t
0
.
8
1
C
o
n
s
i
s
t
e
n
c
y
o
f
t
e
s
t
e
s
(
T
o
n
o
m
e
t
e
r
r
a
t
i
o
s
)
H
a
h
n
e
t
a
l
.
(
1
9
6
9
b
)
C
a
t
t
l
e
;
d
a
i
r
y
b
u
l
l
s
1
7
2
2
m
o
3
4
4
2
m
o
7
2
1
5
0
m
o
l
%
n
o
r
m
a
l
s
p
e
r
m
%
m
o
t
i
l
e
%
n
o
r
m
a
l
s
p
e
r
m
%
m
o
t
i
l
e
%
n
o
r
m
a
l
s
p
e
r
m
%
m
o
t
i
l
e
0
.
6
6
0
.
8
0
0
.
7
4
0
.
7
4
0
.
6
3
0
.
6
8
U
s
i
n
g
a
t
o
n
o
m
e
t
e
r
t
o
p
r
o
v
i
d
e
s
i
m
p
l
e
o
b
j
e
c
t
i
v
e
m
e
a
s
u
r
e
m
e
n
t
(
H
a
h
n
e
t
a
l
.
1
9
6
9
a
)
.
B
u
l
l
s
e
j
a
c
u
l
a
t
e
d
4
t
i
m
e
s
w
e
e
k
u
n
d
e
r
i
d
e
a
l
e
x
p
e
r
i
m
e
n
t
a
l
c
o
n
d
i
t
i
o
n
s
(
H
a
h
n
e
t
a
l
.
1
9
6
9
a
)
S
C
H
o
l
r
o
y
d
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
;
B
2
4
y
e
a
r
l
C
a
l
f
o
u
t
p
u
t
0
.
3
3
n
=
1
1
9
E
x
t
e
n
s
i
v
e
g
r
a
z
i
n
g
m
a
n
a
g
e
m
e
n
t
a
n
d
m
u
l
t
i
p
l
e
s
i
r
e
m
a
t
i
n
g
s
%
m
o
t
i
l
e
s
p
e
r
m
H
o
l
r
o
y
d
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
;
B
5
8
B
2
4
y
e
a
r
l
C
a
l
f
o
u
t
p
u
t
0
.
3
9
0
.
5
0
E
x
t
e
n
s
i
v
e
g
r
a
z
i
n
g
m
a
n
a
g
e
m
e
n
t
a
n
d
m
u
l
t
i
p
l
e
s
i
r
e
m
a
t
i
n
g
s
n
=
1
1
9
n
=
2
5
%
n
o
r
m
a
l
s
p
e
r
m
H
o
l
r
o
y
d
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
;
B
S
G
2
4
y
e
a
r
l
C
a
l
f
o
u
t
p
u
t
0
.
6
4
0
.
3
7
E
x
t
e
n
s
i
v
e
g
r
a
z
i
n
g
m
a
n
a
g
e
m
e
n
t
a
n
d
m
u
l
t
i
p
l
e
s
i
r
e
m
a
t
i
n
g
s
n
=
1
1
9
n
=
9
2
%
a
b
n
o
r
m
a
l
m
i
d
-
p
i
e
c
e
s
H
o
l
r
o
y
d
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
;
B
2
4
y
e
a
r
l
C
a
l
f
o
u
t
p
u
t
0
.
2
7
n
=
1
1
9
E
x
t
e
n
s
i
v
e
g
r
a
z
i
n
g
m
a
n
a
g
e
m
e
n
t
a
n
d
m
u
l
t
i
p
l
e
s
i
r
e
m
a
t
i
n
g
s
T
a
b
l
e
1
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
M
a
l
e
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
H
o
r
m
o
n
e
s
G
n
R
H
-
s
t
i
m
u
l
a
t
e
d
t
e
s
t
o
s
t
e
r
o
n
e
P
o
s
t
e
t
a
l
.
(
1
9
8
7
)
C
a
t
t
l
e
;
H
S
h
,
Z
X
1
7
2
9
m
o
s
m
C
a
l
f
o
u
t
p
u
t
R
a
n
k
i
n
g
i
s
s
a
m
e
i
n
2
g
e
n
o
t
y
p
e
s
,
H
S
h
a
n
d
Z
x
,
n
=
4
a
n
d
n
=
3
,
r
e
s
p
e
c
t
i
v
e
l
y
M
c
C
o
s
k
e
r
e
t
a
l
.
(
1
9
8
9
)
C
a
t
t
l
e
;
B
a
d
u
l
t
s
m
C
a
l
f
o
u
t
p
u
t
s
u
m
m
e
r
C
a
l
f
o
u
t
p
u
t
w
i
n
t
e
r
0
.
4
4
n
s
)
0
.
6
0
n
s
S
m
a
l
l
g
r
o
u
p
s
o
f
b
u
l
l
s
p
r
o
d
u
c
e
d
d
i
e
r
i
n
g
s
e
a
s
o
n
a
l
r
e
s
p
o
n
s
e
s
t
o
t
h
i
s
t
e
s
t
i
.
e
.
v
a
r
i
a
b
i
l
i
t
y
i
n
c
r
e
a
s
e
d
b
y
t
h
i
s
e
e
c
t
I
n
h
i
b
i
n
(
s
e
r
u
m
)
S
t
e
w
a
r
t
a
n
d
R
o
s
e
r
(
1
9
9
8
)
H
o
r
s
e
2
m
o
2
5
y
e
a
r
s
m
N
o
c
h
a
n
g
e
d
u
r
i
n
g
f
e
r
t
i
l
e
s
e
a
s
o
n
N
o
d
i
e
r
e
n
c
e
i
n
s
u
b
f
e
r
t
i
l
e
m
a
l
e
s
n
=
5
1
t
o
t
a
l
,
n
=
6
f
e
r
t
i
l
e
,
n
=
3
s
u
b
f
e
r
t
i
l
e
,
n
=
3
i
n
f
e
r
t
i
l
e
I
n
h
i
b
i
n
(
i
n
t
r
a
t
e
s
t
i
c
u
l
a
r
)
S
t
e
w
a
r
t
a
n
d
R
o
s
e
r
(
1
9
9
8
)
H
o
r
s
e
2
m
o
2
5
y
e
a
r
b
s
d
u
r
i
n
g
f
e
r
t
i
l
e
p
e
r
i
o
d
s
N
o
d
i
e
r
e
n
c
e
i
n
s
u
b
f
e
r
t
i
l
e
m
a
l
e
s
n
=
5
1
t
o
t
a
l
,
n
=
6
f
e
r
t
i
l
e
,
n
=
3
s
u
b
f
e
r
t
i
l
e
,
n
=
3
i
n
f
e
r
t
i
l
e
S
e
m
i
n
a
l
p
r
o
t
e
i
n
s
a
n
d
f
a
c
t
o
r
s
H
e
p
a
r
i
n
-
b
i
n
d
i
n
g
p
r
o
t
e
i
n
s
(
H
B
P
)
S
p
e
r
m
a
t
t
a
c
h
m
e
n
t
F
i
t
z
p
a
t
r
i
c
k
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
;
B
,
S
G
>
2
y
e
a
r
s
n
C
a
l
f
o
u
t
p
u
t
n
s
n
=
2
7
S
G
b
u
l
l
s
,
n
=
4
6
B
b
u
l
l
s
B
a
s
e
d
o
n
p
r
o
l
e
o
f
3
H
B
P
o
f
3
0
,
2
4
,
2
1
.
5
k
D
a
R
e
l
a
x
i
n
m
o
t
i
l
i
t
y
K
o
h
s
a
k
a
e
t
a
l
.
(
2
0
0
3
)
C
a
t
t
l
e
;
J
a
p
A
d
u
l
t
s
n
M
o
t
i
l
i
t
y
0
.
6
4
n
=
8
>
6
0
%
m
o
t
i
l
i
t
y
;
n
=
5
<
6
0
%
m
o
t
i
l
i
t
y
F
e
r
t
i
l
i
t
y
-
a
s
s
o
c
i
a
t
e
d
p
r
o
t
e
i
n
s
(
2
D
-
e
l
e
c
t
r
o
p
h
o
r
e
s
i
s
)
K
i
l
l
i
a
n
e
t
a
l
.
(
1
9
9
3
)
C
a
t
t
l
e
;
H
o
A
d
u
l
t
s
n
A
I
f
e
r
t
i
l
i
t
y
(
r
e
c
o
r
d
s
)
(
i
n
d
e
x
o
f
4
p
r
o
t
e
i
n
s
)
0
.
8
9
n
=
3
5
H
i
g
h
f
e
r
t
i
l
i
t
y
2
6
k
D
a
,
5
5
k
D
a
.
L
o
w
f
e
r
t
i
l
i
t
y
1
6
k
D
a
,
1
6
k
D
a
B
r
a
n
d
o
n
e
t
a
l
.
(
1
9
9
9
)
H
o
r
s
e
A
d
u
l
t
s
n
C
o
r
r
e
l
a
t
e
d
w
i
t
h
f
o
a
l
g
e
t
t
i
n
g
a
b
i
l
i
t
y
S
P
-
1
S
P
-
2
S
P
-
3
S
P
-
4
0
.
8
4
)
0
.
8
7
)
0
.
8
5
)
0
.
8
8
n
=
6
S
P
-
1
(
7
2
k
D
a
)
c
r
o
s
s
-
r
e
a
c
t
s
w
i
t
h
b
o
v
i
n
e
o
s
t
e
o
p
o
n
t
i
n
(
5
5
k
D
a
)
a
n
t
i
b
o
d
i
e
s
M
o
u
r
a
e
t
a
l
.
(
2
0
0
6
)
C
a
t
t
l
e
A
d
u
l
t
s
n
N
R
R
r
e
g
r
e
s
s
i
o
n
e
q
u
a
t
i
o
n
w
i
t
h
1
,
2
,
3
e
q
u
a
t
i
o
n
w
i
t
h
1
,
3
,
4
1
.
s
p
e
r
m
a
d
h
e
s
i
n
2
.
o
s
t
e
o
p
o
n
t
i
n
3
.
B
S
P
3
0
k
D
a
4
.
p
h
o
s
p
h
o
l
i
p
a
s
e
A
2
0
.
7
5
0
.
7
3
a
v
.
i
n
d
i
v
i
d
u
a
l
0
.
4
2
n
=
3
7
b
u
l
l
s
,
m
a
n
y
i
n
s
e
m
i
n
a
t
i
o
n
s
O
s
t
e
o
p
o
n
t
i
n
(
P
5
5
b
)
A
t
t
a
c
h
m
e
n
t
C
a
n
c
e
l
e
t
a
l
.
(
1
9
9
7
)
C
a
t
t
l
e
;
H
o
A
d
u
l
t
s
n
A
I
f
e
r
t
i
l
i
t
y
0
.
4
8
O
n
e
o
f
K
i
l
l
i
a
n
s
4
f
e
r
t
i
l
i
t
y
-
a
s
s
o
c
i
a
t
e
d
p
r
o
t
e
i
n
s
.
n
=
2
4
L
i
p
o
c
a
l
i
n
-
t
y
p
e
p
r
o
s
t
a
g
l
a
n
d
i
n
D
2
s
y
n
t
h
a
s
e
(
P
2
6
b
;
P
3
1
b
)
P
r
o
s
t
a
g
l
a
n
d
i
n
s
y
n
t
h
e
s
i
s
G
e
r
e
n
a
e
t
a
l
.
(
1
9
9
8
)
C
a
t
t
l
e
;
H
o
A
d
u
l
t
s
n
S
p
e
c
u
l
a
t
e
t
h
a
t
t
h
i
s
p
r
o
t
e
i
n
m
a
y
p
l
a
y
a
n
i
m
p
o
r
t
a
n
t
r
o
l
e
i
n
b
o
t
h
d
e
v
e
l
o
p
m
e
n
t
a
n
d
m
a
t
u
r
a
t
i
o
n
o
f
s
p
e
r
m
O
n
e
o
f
K
i
l
l
i
a
n
s
o
r
i
g
i
n
a
l
f
e
r
t
i
l
i
t
y
-
a
s
s
o
c
i
a
t
e
d
p
r
o
t
e
i
n
s
.
P
r
o
t
e
i
n
i
d
e
n
t
i
c
a
t
i
o
n
T
a
b
l
e
1
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
M
a
l
e
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
F
o
u
c
h
e
c
o
u
r
t
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
;
H
o
,
a
n
d
S
h
e
e
p
A
d
u
l
t
s
n
F
e
r
t
i
l
i
t
y
r
a
t
e
o
f
s
u
c
c
e
s
s
a
f
t
e
r
a
r
t
i
c
i
a
l
i
n
s
e
m
i
n
a
t
i
o
n
N
o
c
o
r
r
e
l
a
t
i
o
n
n
s
n
=
1
3
3
b
u
l
l
s
n
o
t
n
e
c
e
s
s
a
r
y
f
o
r
m
a
l
e
f
e
r
t
i
l
i
t
y
o
r
a
s
s
u
m
e
d
b
y
o
t
h
e
r
p
r
o
t
e
i
n
s
n
=
6
5
r
a
m
s
G
a
t
t
i
e
t
a
l
.
(
2
0
0
4
)
R
e
v
i
e
w
V
a
r
i
o
u
s
m
a
m
m
a
l
i
a
n
s
p
e
c
i
e
s
A
d
u
l
t
s
n
A
r
g
u
e
s
t
h
i
s
i
s
n
o
t
a
g
o
o
d
f
e
r
t
i
l
i
t
y
m
a
r
k
e
r
l
o
w
i
n
l
o
w
f
e
r
t
i
l
i
t
y
b
u
t
a
l
s
o
o
f
t
e
n
l
o
w
i
n
h
i
g
h
f
e
r
t
i
l
i
t
y
H
e
a
t
s
h
o
c
k
p
r
o
t
e
i
n
7
0
(
H
S
P
7
0
)
A
t
t
a
c
h
m
e
n
t
E
m
b
r
y
o
d
e
v
e
l
o
p
m
e
n
t
M
a
t
w
e
e
e
t
a
l
.
(
2
0
0
1
)
C
a
t
t
l
e
A
d
u
l
t
s
p
S
p
e
r
m
a
t
t
a
c
h
m
e
n
t
r
e
d
u
c
e
d
b
y
a
n
t
i
b
o
d
y
(
p
<
0
.
0
5
)
I
n
v
i
t
r
o
S
p
i
n
a
c
i
e
t
a
l
.
(
2
0
0
5
)
P
i
g
A
d
u
l
t
s
p
A
n
t
i
b
o
d
y
r
e
d
u
c
e
d
I
V
F
(
p
<
0
.
0
5
)
I
n
v
i
t
r
o
S
p
e
r
m
m
e
m
b
r
a
n
e
a
n
t
i
g
e
n
(
P
2
5
b
)
A
t
t
a
c
h
m
e
n
t
P
a
r
e
n
t
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
A
d
u
l
t
s
p
8
1
1
s
u
b
f
e
r
t
i
l
e
h
a
d
l
o
w
P
2
5
b
8
8
f
e
r
t
i
l
e
h
a
d
h
i
g
h
P
2
5
b
A
I
f
e
r
t
i
l
i
t
y
a
s
c
o
r
r
e
c
t
e
d
N
R
R
s
c
o
r
e
d
1
9
s
u
b
f
e
r
t
i
l
e
<
5
;
f
e
r
t
i
l
e
5
9
P
l
a
t
e
l
e
t
a
c
t
i
v
a
t
i
n
g
f
a
c
t
o
r
(
P
A
F
)
S
p
e
r
m
m
o
t
i
l
i
t
y
S
p
e
r
m
c
a
p
a
c
i
t
a
t
i
o
n
R
o
u
d
e
b
u
s
h
a
n
d
D
i
e
h
l
(
2
0
0
1
)
P
i
g
A
d
u
l
t
s
p
F
a
r
r
o
w
i
n
g
r
a
t
e
n
u
m
b
e
r
p
i
g
l
e
t
s
b
o
r
n
l
i
t
t
e
r
s
i
z
e
0
.
6
1
n
=
1
4
B
r
a
c
k
e
t
t
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
A
d
u
l
t
s
n
C
o
r
r
.
m
o
t
i
l
i
t
y
c
o
r
r
.
c
o
n
c
e
p
t
i
o
n
r
a
t
e
(
p
<
0
.
0
5
)
n
=
8
N
R
R
0
.
4
0
A
b
s
t
r
a
c
t
p
o
s
t
e
r
p
r
e
s
e
n
t
a
t
i
o
n
.
i
n
t
r
a
c
e
l
l
u
l
a
r
C
a
2
+
R
o
u
d
e
b
u
s
h
e
t
a
l
.
(
2
0
0
5
)
P
r
i
m
a
t
e
A
d
u
l
t
s
n
d
u
r
i
n
g
b
r
e
e
d
i
n
g
s
e
a
s
o
n
c
o
r
r
.
m
o
t
i
l
i
t
y
A
b
s
t
r
a
c
t
o
n
l
y
B
o
v
i
n
e
s
e
m
i
n
a
l
p
l
a
s
m
a
p
r
o
t
e
i
n
A
3
(
B
S
P
-
A
3
)
S
p
e
r
m
d
e
c
a
p
a
c
i
t
a
t
i
o
n
R
o
n
c
o
l
e
t
t
a
e
t
a
l
.
(
2
0
0
6
)
C
a
t
t
l
e
;
N
A
d
u
l
t
s
n
i
n
h
i
g
h
-
f
e
r
t
i
l
i
t
y
g
r
o
u
p
n
=
2
0
,
h
i
g
h
f
e
r
t
i
l
i
t
y
n
=
3
,
l
o
w
f
e
r
t
i
l
i
t
y
n
=
4
A
c
i
d
s
e
m
i
n
a
l
u
i
d
p
r
o
t
e
i
n
(
a
S
F
P
)
S
p
e
r
m
d
e
c
a
p
a
c
i
t
a
t
i
o
n
S
p
e
r
m
s
t
r
u
c
t
u
r
a
l
p
r
o
t
e
i
n
C
h
r
o
m
a
t
i
n
c
o
n
d
e
n
s
a
t
i
o
n
R
o
n
c
o
l
e
t
t
a
e
t
a
l
.
(
2
0
0
6
)
C
a
t
t
l
e
;
N
A
d
u
l
t
s
n
i
n
h
i
g
h
-
f
e
r
t
i
l
i
t
y
g
r
o
u
p
n
=
2
0
,
h
i
g
h
f
e
r
t
i
l
i
t
y
n
=
3
,
l
o
w
f
e
r
t
i
l
i
t
y
n
=
4
F
e
r
t
i
l
i
t
y
-
a
s
s
o
c
i
a
t
e
d
a
n
t
i
g
e
n
(
F
A
A
)
(
D
N
a
s
e
)
H
e
p
a
r
i
n
-
b
i
n
d
i
n
g
p
r
o
t
e
i
n
B
e
l
l
i
n
e
t
a
l
.
(
1
9
9
8
)
C
a
t
t
l
e
;
S
G
,
S
C
A
d
u
l
t
E
x
p
t
.
1
E
x
p
t
.
2
s
p
F
e
r
t
i
l
i
t
y
a
v
e
r
a
g
e
F
A
A
+
=
8
8
%
F
A
A
)
=
7
9
%
F
A
A
+
=
8
7
%
(
n
=
1
2
)
F
A
A
)
=
7
8
%
(
n
=
6
)
O
f
2
1
9
1
b
u
l
l
s
8
8
%
p
o
s
i
t
i
v
e
f
o
r
F
A
A
n
=
1
0
5
b
u
l
l
s
e
x
p
t
1
(
p
<
0
.
0
1
)
E
x
p
e
r
i
m
e
n
t
2
b
u
l
l
s
w
i
t
h
h
i
g
h
s
e
r
v
i
n
g
c
a
p
a
c
i
t
y
S
p
r
o
t
t
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
A
d
u
l
t
H
e
r
d
1
H
e
r
d
2
H
e
r
d
3
s
n
A
I
P
R
s
i
n
g
l
e
s
e
r
v
e
F
A
A
+
=
7
4
%
F
A
A
)
=
6
7
%
F
A
A
+
=
2
5
%
F
A
A
)
=
1
6
%
F
A
A
+
=
7
5
%
F
A
A
)
=
6
8
%
n
=
2
5
b
u
l
l
s
T
a
b
l
e
1
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
M
a
l
e
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
A
r
a
c
h
i
d
o
n
a
t
e
1
5
-
l
i
p
o
x
y
g
e
n
a
s
e
(
L
O
X
)
M
a
r
k
e
r
f
o
r
s
p
e
r
m
c
y
t
o
p
l
a
s
m
i
c
d
r
o
p
l
e
t
L
o
v
e
r
c
a
m
p
e
t
a
l
.
(
2
0
0
4
)
P
i
g
A
d
u
l
t
s
p
F
a
r
r
o
w
i
n
g
r
a
t
e
)
0
.
2
5
t
o
)
0
.
6
6
A
b
s
t
r
a
c
t
o
n
l
y
n
=
1
5
F
i
s
c
h
e
r
e
t
a
l
.
(
2
0
0
5
)
P
i
g
A
d
u
l
t
s
p
A
m
o
u
n
t
v
a
r
i
e
s
w
i
t
h
a
m
o
u
n
t
o
f
c
y
t
o
p
l
a
s
m
i
c
d
r
o
p
l
e
t
P
r
o
v
e
d
t
o
b
e
a
c
o
m
p
o
n
e
n
t
o
f
c
y
t
o
p
l
a
s
m
i
c
d
r
o
p
l
e
t
i
n
b
o
a
r
,
m
a
n
,
m
o
u
s
e
a
n
d
s
t
a
l
l
i
o
n
.
n
=
8
U
b
i
q
u
i
t
i
n
(
u
b
i
q
u
i
t
i
n
-
l
a
b
e
l
l
e
d
s
p
e
r
m
p
r
o
t
e
i
n
s
)
M
a
r
k
e
r
d
e
g
r
a
d
e
d
p
r
o
t
e
i
n
s
Z
o
n
a
p
e
n
e
t
r
a
t
i
o
n
S
u
t
o
v
s
k
y
(
2
0
0
3
)
H
o
r
s
e
A
d
u
l
t
s
n
A
n
i
m
a
l
s
i
n
s
u
b
f
e
r
t
i
l
e
g
r
o
u
p
h
a
v
e
h
i
g
h
e
r
l
e
v
e
l
s
a
n
d
m
o
r
e
b
a
n
d
s
.
A
n
i
m
a
l
s
i
n
f
e
r
t
i
l
e
g
r
o
u
p
s
i
n
c
r
e
a
s
e
d
u
r
i
n
g
l
o
w
-
f
e
r
t
i
l
i
t
y
s
e
a
s
o
n
a
n
d
l
o
w
e
s
t
a
t
h
i
g
h
e
s
t
f
e
r
t
i
l
i
t
y
s
e
a
s
o
n
n
=
3
f
e
r
t
i
l
e
n
=
1
s
u
b
f
e
r
t
i
l
e
P
h
o
s
p
h
o
l
i
p
i
d
h
y
d
r
o
p
e
r
o
x
i
d
e
g
l
u
t
a
t
h
i
o
n
e
p
e
r
o
x
i
d
a
s
e
(
P
H
G
P
x
,
s
e
l
e
n
o
p
r
o
t
e
i
n
)
A
n
t
i
o
x
i
d
a
n
t
S
p
e
r
m
s
t
r
u
c
t
u
r
a
l
p
r
o
t
e
i
n
F
o
r
e
s
t
a
e
t
a
l
.
(
2
0
0
2
)
H
u
m
a
n
A
d
u
l
t
s
p
S
p
e
r
m
v
i
a
b
i
l
i
t
y
S
p
e
r
m
i
n
t
e
g
r
i
t
y
S
p
e
r
m
m
o
t
i
l
i
t
y
0
.
3
5
0
.
4
4
0
.
4
5
S
o
l
e
s
p
e
r
m
c
o
m
p
o
n
e
n
t
c
o
n
t
a
i
n
i
n
g
s
e
l
e
n
i
u
m
.
S
e
l
e
n
i
u
m
d
e
c
i
e
n
c
y
=
i
n
f
e
r
t
i
l
i
t
y
.
n
=
7
5
i
n
f
e
r
t
i
l
e
n
=
3
7
f
e
r
t
i
l
e
A
l
s
o
b
u
l
l
s
,
b
o
a
r
s
,
s
t
a
l
l
i
o
n
s
d
o
g
s
u
n
p
u
b
l
i
s
h
e
d
1
1
b
-
H
y
d
r
o
x
y
s
t
e
r
o
i
d
d
e
h
y
d
r
o
g
e
n
a
s
e
M
i
c
h
a
e
l
e
t
a
l
.
(
2
0
0
3
)
R
e
v
i
e
w
M
a
m
m
a
l
s
a
n
d
b
a
c
t
e
r
i
a
S
p
e
r
m
a
t
o
g
e
n
e
s
i
s
I
s
o
z
y
m
e
s
h
a
v
e
r
o
l
e
i
n
c
o
n
t
r
o
l
l
i
n
g
t
h
e
e
e
c
t
o
f
s
t
r
e
s
s
o
n
f
e
r
t
i
l
i
t
y
.
P
r
o
t
a
m
i
n
e
-
1
a
n
d
p
r
o
t
a
m
i
n
e
-
2
S
p
e
r
m
c
h
r
o
m
a
t
i
n
c
o
n
d
e
n
s
a
t
i
o
n
S
t
e
g
e
r
e
t
a
l
.
(
2
0
0
1
)
H
u
m
a
n
A
d
u
l
t
b
s
I
V
F
v
e
r
s
u
s
l
o
w
l
e
v
e
l
s
o
f
p
r
o
t
a
m
i
n
e
m
R
N
A
0
.
7
B
i
o
p
s
y
r
e
q
u
i
r
e
d
t
o
a
c
c
e
s
s
r
o
u
n
d
s
p
e
r
m
a
t
i
d
s
A
,
A
n
g
u
s
;
A
g
e
,
a
g
e
o
f
s
a
m
p
l
i
n
g
i
n
m
o
n
t
h
s
(
m
o
)
;
A
I
,
a
r
t
i
c
i
a
l
i
n
s
e
m
i
n
a
t
i
o
n
;
B
,
B
r
a
h
m
a
n
;
B
r
,
B
r
a
n
g
u
s
;
b
s
,
b
i
o
p
s
y
;
C
,
C
h
a
r
o
l
a
i
s
;
D
r
,
D
r
o
u
g
h
t
m
a
s
t
e
r
;
H
,
H
e
r
e
f
o
r
d
;
H
C
,
H
e
r
e
f
o
r
d
C
h
a
r
o
l
a
i
s
;
H
o
,
H
o
l
s
t
e
i
n
;
H
S
h
,
H
e
r
e
f
o
r
d
S
h
o
r
t
h
o
r
n
;
I
V
F
,
i
n
v
i
t
r
o
f
e
r
t
i
l
i
z
a
t
i
o
n
;
J
a
p
,
J
a
p
a
n
e
s
e
b
l
a
c
k
a
n
d
J
a
p
a
n
e
s
e
S
h
o
r
t
h
o
r
n
;
l
,
l
i
v
e
a
n
i
m
a
l
m
e
a
s
u
r
e
m
e
n
t
;
N
,
N
e
l
o
r
e
;
n
,
s
a
m
p
l
e
n
u
m
b
e
r
;
N
R
R
,
n
o
n
-
r
e
t
u
r
n
r
a
t
e
;
n
s
,
n
o
t
s
i
g
n
i
c
a
n
t
(
p
>
0
.
0
5
)
;
P
R
,
p
r
e
g
n
a
n
c
y
r
a
t
e
;
r
g
,
g
e
n
e
t
i
c
c
o
r
r
e
l
a
t
i
o
n
;
r
p
,
p
h
e
n
o
t
y
p
i
c
c
o
r
r
e
l
a
t
i
o
n
;
S
C
,
s
c
r
o
t
a
l
c
i
r
c
u
m
f
e
r
e
n
c
e
(
o
r
d
i
a
m
e
t
e
r
)
;
S
C
r
,
S
a
n
t
a
C
r
u
z
;
S
G
,
S
a
n
t
a
G
e
r
t
r
u
d
i
s
;
s
m
,
s
e
r
u
m
;
s
n
,
s
e
m
e
n
;
s
p
,
s
p
e
r
m
;
Z
X
,
z
e
b
u
c
r
o
s
s
.
T
a
b
l
e
2
.
M
a
l
e
p
h
e
n
o
t
y
p
i
c
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
a
n
d
t
h
e
i
r
c
o
r
r
e
l
a
t
e
d
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
i
n
f
e
m
a
l
e
p
r
o
g
e
n
y
(
a
)
P
r
e
-
p
u
b
e
r
t
a
l
t
r
a
i
t
s
;
(
b
)
P
o
s
t
-
p
u
b
e
r
t
a
l
t
r
a
i
t
s
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
F
e
m
a
l
e
P
r
o
g
e
n
y
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
(
a
)
P
r
e
-
p
u
b
e
r
t
a
l
t
r
a
i
t
s
C
o
r
r
e
c
t
e
d
S
C
(
S
C
A
g
e
)
B
r
i
n
k
s
e
t
a
l
.
(
1
9
7
8
)
C
a
t
t
l
e
;
H
,
A
1
2
m
o
l
A
g
e
o
f
p
u
b
e
r
t
y
)
0
.
7
1
)
0
.
3
6
K
i
n
g
e
t
a
l
.
(
1
9
8
3
)
C
a
t
t
l
e
;
H
1
2
m
o
l
A
g
e
o
f
p
u
b
e
r
t
y
)
1
.
0
7
A
r
e
v
i
e
w
o
f
d
a
t
a
t
o
1
9
8
8
l
i
n
k
i
n
g
1
2
m
o
n
t
h
S
C
t
o
v
a
r
i
o
u
s
p
a
r
a
m
e
t
e
r
s
o
f
g
r
o
w
t
h
a
n
d
r
e
p
r
o
d
u
c
t
i
o
n
P
e
r
r
y
e
t
a
l
.
(
1
9
9
0
b
)
C
a
t
t
l
e
;
G
A
,
A
X
,
B
X
,
G
B
,
H
S
h
,
A
X
B
X
,
B
X
A
X
1
6
m
o
l
A
g
e
o
f
p
u
b
e
r
t
y
n
s
6
g
e
n
o
t
y
p
e
s
n
=
2
6
s
i
r
e
s
n
=
2
8
5
f
e
m
a
l
e
s
a
n
d
5
1
m
a
l
e
s
V
a
r
g
a
s
e
t
a
l
.
(
1
9
9
8
)
C
a
t
t
l
e
;
B
1
8
m
o
l
A
g
e
o
f
p
u
b
e
r
t
y
)
0
.
3
2
n
=
2
8
m
a
l
e
s
n
=
2
6
1
f
e
m
a
l
e
s
M
a
r
t
i
n
e
z
-
V
e
l
a
z
q
u
e
z
e
t
a
l
.
(
2
0
0
3
)
C
a
t
t
l
e
;
H
,
A
,
R
,
L
,
S
,
C
,
P
,
G
,
B
v
h
,
M
A
R
C
I
,
I
I
&
I
I
I
1
2
m
o
l
A
g
e
o
f
p
u
b
e
r
t
y
)
0
.
1
5
n
>
7
0
0
0
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
2
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
m
o
1
1
m
o
1
3
m
o
l
S
t
a
n
d
a
r
d
a
g
e
1
s
t
o
e
s
t
r
u
s
S
t
a
n
d
a
r
d
a
g
e
1
s
t
o
e
s
t
r
u
s
S
t
a
n
d
a
r
d
a
g
e
1
s
t
o
e
s
t
r
u
s
0
.
1
5
0
.
2
0
)
0
.
2
8
0
.
2
1
)
0
.
4
6
0
.
2
3
C
r
o
s
s
-
b
r
e
e
d
i
n
g
e
x
p
e
r
i
m
e
n
t
f
o
l
l
o
w
s
o
n
i
n
l
a
t
e
r
y
e
a
r
s
.
B
a
s
e
d
o
n
H
a
n
d
A
w
i
t
h
o
t
h
e
r
B
r
i
t
i
s
h
b
r
e
e
d
s
.
n
=
2
3
4
s
i
r
e
g
r
o
u
p
s
o
f
a
b
o
u
t
6
m
a
l
e
s
a
n
d
6
f
e
m
a
l
e
s
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
3
)
C
a
t
t
l
e
;
A
9
1
3
m
o
1
3
m
o
l
S
t
a
n
d
a
r
d
a
g
e
1
s
t
o
e
s
t
r
u
s
S
t
a
n
d
a
r
d
a
g
e
1
s
t
o
e
s
t
r
u
s
)
0
.
4
0
0
.
2
9
)
0
.
5
0
0
.
2
9
C
o
n
t
i
n
u
e
d
f
r
o
m
p
r
e
v
i
o
u
s
s
t
u
d
y
b
u
t
r
u
n
o
n
s
e
p
a
r
a
t
e
p
r
o
p
e
r
t
y
.
n
=
5
5
0
c
o
w
s
m
a
t
e
d
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
1
3
m
o
l
S
t
a
n
d
a
r
d
a
g
e
1
s
t
o
e
s
t
r
u
s
s
i
t
e
1
S
t
a
n
d
a
r
d
a
g
e
1
s
t
o
e
s
t
r
u
s
s
i
t
e
2
)
0
.
1
9
)
0
.
2
1
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
s
t
u
d
i
e
s
a
t
2
s
i
t
e
s
.
B
y
n
o
w
h
a
v
e
l
o
n
g
h
i
s
t
o
r
y
o
f
s
e
l
e
c
t
i
o
n
e
c
t
s
C
o
r
r
e
c
t
e
d
S
C
(
S
C
A
g
e
)
S
m
i
t
h
e
t
a
l
.
(
1
9
8
9
b
)
C
a
t
t
l
e
;
H
,
A
1
2
m
o
l
A
g
e
1
s
t
c
a
l
f
)
0
.
8
3
A
l
l
o
w
a
n
c
e
s
m
a
d
e
f
o
r
i
n
b
r
e
e
d
i
n
g
o
f
h
e
r
d
M
a
r
t
i
n
e
z
-
V
e
l
a
z
q
u
e
z
e
t
a
l
.
(
2
0
0
3
)
C
a
t
t
l
e
;
H
,
A
,
H
,
A
,
R
,
L
,
S
,
C
,
P
,
G
,
B
v
h
,
M
A
R
C
I
,
I
I
&
I
I
I
1
2
m
o
l
A
g
e
1
s
t
c
a
l
f
0
.
1
5
n
>
7
0
0
0
M
e
y
e
r
e
t
a
l
.
(
1
9
9
1
)
C
a
t
t
l
e
;
H
A
Z
X
1
2
2
4
m
o
l
D
a
y
s
t
o
c
a
l
v
i
n
g
D
a
y
s
t
o
c
a
l
v
i
n
g
D
a
y
s
t
o
c
a
l
v
i
n
g
)
0
.
2
5
)
0
.
2
8
)
0
.
4
1
D
a
t
a
f
r
o
m
v
a
r
i
o
u
s
s
o
u
r
c
e
s
.
V
a
r
i
a
b
l
e
a
g
e
a
r
o
u
n
d
a
b
o
u
t
p
u
b
e
r
t
y
.
S
o
m
e
o
l
d
e
r
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
1
3
m
o
l
C
a
l
v
i
n
g
d
a
t
e
s
i
t
e
1
C
a
l
v
i
n
g
d
a
t
e
s
i
t
e
2
)
0
.
0
6
)
0
.
2
5
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
a
t
2
s
i
t
e
s
.
B
y
n
o
w
h
a
v
e
l
o
n
g
h
i
s
t
o
r
y
o
f
s
e
l
e
c
t
i
o
n
e
c
t
s
M
e
y
e
r
a
n
d
J
o
h
n
s
t
o
n
(
2
0
0
1
)
C
a
t
t
l
e
;
B
1
0
2
6
m
o
l
D
a
y
s
t
o
c
a
l
v
i
n
g
)
0
.
3
M
o
d
e
l
l
e
d
d
a
t
a
o
n
l
y
,
n
o
n
e
o
f
o
r
i
g
i
n
a
l
d
a
t
a
g
i
v
e
n
C
o
r
r
e
c
t
e
d
S
C
(
S
C
A
g
e
)
M
o
r
r
i
s
a
n
d
C
u
l
l
e
n
(
1
9
9
4
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
m
o
1
1
m
o
1
3
m
o
l
Y
e
a
r
l
i
n
g
p
r
e
g
n
a
n
c
y
r
a
t
e
0
.
5
3
0
.
6
1
0
.
3
4
0
.
5
9
0
.
5
7
0
.
7
7
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
s
t
u
d
i
e
s
.
N
e
w
s
i
t
e
.
M
u
l
t
i
p
l
e
b
r
e
e
d
s
a
n
d
c
r
o
s
s
e
s
E
v
a
n
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
1
2
m
o
l
H
e
i
f
e
r
p
r
e
g
n
a
n
c
y
r
a
t
e
0
.
0
0
2
0
.
4
5
n
=
1
2
2
0
b
u
l
l
s
.
P
r
e
g
n
a
n
c
y
a
s
y
e
s
o
r
n
o
E
l
e
r
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
;
N
1
5
m
o
l
Y
e
a
r
l
i
n
g
p
r
e
g
n
a
n
c
y
r
a
t
e
0
.
2
0
0
.
1
3
n
=
2
5
,
4
6
6
C
o
r
r
e
c
t
e
d
S
C
(
S
C
A
g
e
)
T
o
e
l
l
e
a
n
d
R
o
b
i
s
o
n
(
1
9
8
5
)
C
a
t
t
l
e
;
H
6
.
5
m
o
1
2
m
o
l
L
i
f
e
t
i
m
e
p
r
e
g
n
a
n
c
y
r
a
t
e
L
i
f
e
t
i
m
e
p
r
e
g
n
a
n
c
y
r
a
t
e
0
.
9
9
0
.
9
3
M
o
r
r
i
s
a
n
d
C
u
l
l
e
n
(
1
9
9
4
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
m
o
1
1
m
o
1
3
m
o
l
L
i
f
e
t
i
m
e
p
r
e
g
n
a
n
c
y
r
a
t
e
L
i
f
e
t
i
m
e
p
r
e
g
n
a
n
c
y
r
a
t
e
L
i
f
e
t
i
m
e
p
r
e
g
n
a
n
c
y
r
a
t
e
0
.
3
0
0
.
3
7
0
.
4
8
0
.
4
6
0
.
3
5
0
.
4
5
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
s
t
u
d
i
e
s
.
N
e
w
s
i
t
e
.
M
u
l
t
i
p
l
e
b
r
e
e
d
s
a
n
d
c
r
o
s
s
e
s
T
a
b
l
e
2
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
F
e
m
a
l
e
P
r
o
g
e
n
y
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
,
A
,
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
1
3
m
o
l
L
i
f
e
t
i
m
e
p
r
e
g
n
a
n
c
y
r
a
t
e
s
i
t
e
1
L
i
f
e
t
i
m
e
p
r
e
g
n
a
n
c
y
r
a
t
e
s
i
t
e
2
0
.
3
4
0
.
1
4
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
a
t
2
s
i
t
e
s
.
B
y
n
o
w
h
a
v
e
l
o
n
g
h
i
s
t
o
r
y
o
f
s
e
l
e
c
t
i
o
n
e
c
t
s
M
w
a
n
s
a
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
F
1
H
A
,
F
1
C
H
,
F
1
C
A
,
F
1
C
S
h
,
F
1
S
i
H
,
F
1
S
i
A
,
F
1
S
i
S
h
,
F
1
L
H
,
F
1
L
A
,
F
1
L
S
h
1
2
m
o
l
L
i
f
e
t
i
m
e
p
r
e
g
n
a
n
c
y
r
a
t
e
)
0
.
2
5
)
0
.
0
8
M
u
l
t
i
p
l
e
b
r
e
e
d
s
a
n
d
c
r
o
s
s
e
s
P
u
r
v
i
s
e
t
a
l
.
(
1
9
8
8
)
S
h
e
e
p
5
m
o
(
s
h
e
e
p
)
l
O
v
u
l
a
t
i
o
n
r
a
t
e
d
a
m
-
s
o
n
O
v
u
l
a
t
i
o
n
r
a
t
e
-
h
a
l
f
s
i
b
0
.
3
8
0
.
1
7
0
.
2
8
0
.
2
3
C
o
r
r
e
c
t
e
d
S
C
(
S
C
A
g
e
)
M
o
r
r
i
s
a
n
d
C
u
l
l
e
n
(
1
9
9
4
)
C
a
t
t
l
e
;
H
,
A
,
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
m
o
1
1
m
o
1
3
m
o
l
L
i
f
e
t
i
m
e
c
a
l
f
p
r
o
d
u
c
t
i
o
n
L
i
f
e
t
i
m
e
c
a
l
f
p
r
o
d
u
c
t
i
o
n
L
i
f
e
t
i
m
e
c
a
l
f
p
r
o
d
u
c
t
i
o
n
)
0
.
0
9
0
.
4
5
0
.
0
3
0
.
5
1
0
.
0
8
0
.
5
5
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
s
t
u
d
i
e
s
.
N
e
w
s
i
t
e
.
M
u
l
t
i
p
l
e
b
r
e
e
d
s
a
n
d
c
r
o
s
s
e
s
B
a
m
u
a
l
i
m
e
t
a
l
.
(
1
9
8
4
)
C
a
t
t
l
e
;
D
r
2
7
y
e
a
r
l
E
B
V
f
e
r
t
i
l
i
t
y
n
s
P
o
s
t
-
p
u
b
e
r
t
a
l
P
e
r
c
e
n
t
n
o
r
m
a
l
s
p
e
r
m
B
r
i
n
k
s
e
t
a
l
.
(
1
9
7
8
)
C
a
t
t
l
e
;
H
,
A
1
2
m
o
l
A
g
e
o
f
p
u
b
e
r
t
y
)
0
.
3
7
O
n
l
y
%
n
o
r
m
a
l
s
p
e
r
m
f
a
v
o
u
r
a
b
l
y
c
o
r
r
e
l
a
t
e
d
w
i
t
h
a
g
e
o
f
p
u
b
e
r
t
y
.
%
p
r
i
m
a
r
y
a
b
n
o
r
m
a
l
i
t
i
e
s
,
%
s
e
c
o
n
d
a
r
y
a
b
n
o
r
m
a
l
i
t
i
e
s
a
n
d
m
o
t
i
l
i
t
y
n
o
t
f
a
v
o
u
r
a
b
l
y
c
o
r
r
e
l
a
t
e
d
w
i
t
h
a
g
e
o
f
p
u
b
e
r
t
y
G
n
R
H
-
s
t
i
m
u
l
a
t
e
d
L
H
H
a
l
e
y
e
t
a
l
.
(
1
9
8
9
)
S
h
e
e
p
2
.
5
5
m
o
s
m
a
g
e
o
e
s
t
r
u
s
o
v
u
l
a
t
i
o
n
I
G
F
-
1
G
o
n
g
e
t
a
l
.
(
1
9
9
1
)
C
a
t
t
l
e
;
H
x
1
2
m
o
s
m
T
r
e
a
t
e
d
G
H
t
o
i
n
c
r
e
a
s
e
I
G
F
-
1
l
a
r
g
e
f
o
l
l
i
c
l
e
s
p
<
0
.
0
0
1
O
e
s
t
r
a
d
i
o
l
n
s
P
r
o
g
e
s
t
e
r
o
n
e
n
s
F
S
H
n
s
L
H
n
s
L
H
p
u
l
s
e
f
r
e
q
u
e
n
c
y
n
s
F
S
H
,
L
H
r
e
c
e
p
t
o
r
s
n
s
n
=
1
2
A
r
g
u
m
e
n
t
f
o
r
d
i
r
e
c
t
e
e
c
t
s
o
f
I
G
F
-
1
C
h
a
s
e
e
t
a
l
.
(
1
9
9
8
)
C
a
t
t
l
e
;
B
A
d
u
l
t
s
m
d
e
v
e
l
o
p
i
n
g
f
o
l
l
i
c
l
e
s
f
o
l
l
i
c
l
e
g
r
o
w
t
h
c
o
r
p
u
s
l
u
t
e
u
m
g
r
o
w
t
h
p
r
o
g
e
s
t
e
r
o
n
e
n
o
e
e
c
t
F
S
H
,
L
H
,
o
e
s
t
r
a
d
i
o
l
&
p
r
e
-
o
v
u
l
a
t
o
r
y
f
o
l
l
i
c
l
e
s
B
a
s
e
d
o
n
G
H
r
e
c
e
p
t
o
r
-
d
e
c
i
e
n
t
c
a
t
t
l
e
.
n
=
1
6
Y
i
l
m
a
z
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
;
A
5
6
m
o
6
8
m
o
5
6
m
o
6
8
m
o
s
m
A
g
e
1
s
t
c
a
l
f
A
g
e
1
s
t
c
a
l
f
C
a
l
v
i
n
g
r
a
t
e
C
a
l
v
i
n
g
r
a
t
e
)
0
.
1
8
0
.
3
3
)
0
.
2
3
0
.
3
3
)
0
.
4
8
0
.
1
5
)
0
.
4
8
0
.
1
6
0
.
0
2
)
0
.
2
2
0
.
0
2
0
.
0
8
S
e
l
e
c
t
i
o
n
o
f
h
i
g
h
a
n
d
l
o
w
l
i
n
e
s
s
t
a
r
t
e
d
1
9
8
9
1
9
9
0
a
n
d
i
n
b
r
e
e
d
i
n
g
c
o
n
t
i
n
u
e
d
w
i
t
h
n
=
8
b
u
l
l
s
p
e
r
y
e
a
r
a
n
d
n
=
1
0
0
c
o
w
s
p
e
r
y
e
a
r
Although to date the serum concentration of inhibin in
the pre-pubertal bull has not been shown to be a useful
predictor of testicular development (Miyamoto et al.
1989; Lejeune et al. 1997; Matsuzaki et al. 2000; Whea-
ton and Godfrey 2003) (Table 1), theoretically, it may
be of value. This trait requires only a single blood
sample for measurement, and thus, it may be useful to
investigate the relationship between serum inhibin
concentration and testes development and function.
This trait could be readily measured within a testing
schedule for pre-pubertal bulls under industry condi-
tions.
Because they are best undertaken at 35 months of
age, both the GnRH-stimulated LH response test and
measurement of seruminhibin can genuinely be classied
as potential early-life predictor traits of fertility. In dairy
heifers, the GnRH-stimulated LH response has been
shown to be heritable and genetically correlated with the
time of onset of ovulation post-partum (Royal et al.
2000). However, most investigations of these traits have
been conducted in small numbers of Bos taurus and some
tropically adapted bulls (Table 1). Therefore, there is a
need to systematically investigate the usefulness of these
tests in young tropical beef cattle bull genotypes grazed
under semi-extensive tropical production systems to
determine their value as early-life predictors of fertility.
The data presented in the pre-pubertal section of
Table 1 and from other reported research also suggest
that blood serum IGF-1 (Thomas et al. 2002; Yilmaz
et al. 2004) and blood serum leptin (Moschos et al.
2002; Thomas et al. 2002; Boelhauve et al. 2005; Kmiec
et al. 2006; Yong-Jun et al. 2006) measurements are
promising predictors of fertility. IGF-1, measured in
pre-pubertal Bos taurus bulls, was positively correlated
with adult scrotal circumference and sperm motility and
genetically correlated with the age at rst calf of female
progeny and calving rate (Yilmaz et al. 2004). Leptin
has been linked to both male and female reproductive
performance [GnRH pulsatility (Moschos et al. 2002
human); scrotal circumference (Thomas et al. 2002
cattle; Kmiec et al. 2006 pig); per cent and number of
motile sperm (Kmiec et al. 2006); ovulation (Moschos
et al. 2002; Kmiec et al. 2006), ovulation rate (Moschos
et al. 2002), blastocyst implantation (Yong-Jun et al.
2006 mouse) and embryonic development (Boelhauve
et al. 2005 cattle)]. However, despite these promising
relationships, both these hormones have diverse, multi-
ple functions in a number of species (Moschos et al.
2002; Thomas et al. 2002; Yilmaz et al. 2004; Boelhauve
et al. 2005; Kmiec et al. 2006; Yong-Jun et al. 2006) as
reported previously, and this suggests that they may be
facilitators of reproductive development rather than key
controlling factors. Importantly, in the post-pubertal
section of Table 1, it is clear that there is no support in
the literature for serum hormonal measurements being
useful predictors of fertility.
Post-pubertal seminal plasma proteins and other
seminal factors are potential candidate traits, tting with
the review objectives (Table 1). Many of the mechanisms
by which these factors impact on fertility, specically the
fertilizing ability of sperm, are known (Killian et al.
1993; Cancel et al. 1997). Some are moderately corre-
lated with fertility as measured by pregnancy rates or calf T
a
b
l
e
2
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
T
r
a
i
t
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
S
a
m
p
l
e
T
y
p
e
F
e
m
a
l
e
P
r
o
g
e
n
y
C
o
r
r
e
l
a
t
e
d
T
r
a
i
t
s
r
g
r
p
C
o
m
m
e
n
t
s
(
b
)
P
o
s
t
-
p
u
b
e
r
t
a
l
t
r
a
i
t
s
(
>
2
y
e
a
r
s
o
l
d
)
p
r
o
t
e
i
n
s
a
n
d
f
a
c
t
o
r
s
P
l
a
t
e
l
e
t
a
c
t
i
v
a
t
i
n
g
f
a
c
t
o
r
(
P
A
F
)
S
p
e
r
m
m
o
t
i
l
i
t
y
S
p
e
r
m
c
a
p
a
c
i
t
a
t
i
o
n
H
a
r
p
e
r
(
1
9
8
9
)
R
e
v
i
e
w
G
e
n
e
r
a
l
r
e
v
i
e
w
A
d
u
l
t
O
v
u
l
a
t
i
o
n
Z
y
g
o
t
e
U
t
e
r
i
n
e
f
u
n
c
t
i
o
n
s
I
m
p
l
a
n
t
a
t
i
o
n
R
e
f
e
r
e
n
c
e
s
g
i
v
e
o
f
e
x
a
m
p
l
e
s
o
f
P
A
F
l
i
n
k
e
d
t
o
e
m
b
r
y
o
d
e
v
e
l
o
p
m
e
n
t
H
e
a
t
s
h
o
c
k
p
r
o
t
e
i
n
7
0
(
H
S
P
7
0
)
A
t
t
a
c
h
m
e
n
t
E
m
b
r
y
o
d
e
v
e
l
o
p
m
e
n
t
M
a
t
w
e
e
e
t
a
l
.
(
2
0
0
1
)
C
a
t
t
l
e
A
d
u
l
t
s
p
A
n
t
i
b
o
d
i
e
s
i
m
p
a
i
r
e
d
e
m
b
r
y
o
d
e
v
e
l
o
p
m
e
n
t
(
p
<
0
.
0
5
)
I
n
v
i
t
r
o
A
,
A
n
g
u
s
;
A
g
e
,
a
g
e
o
f
s
a
m
p
l
i
n
g
i
n
m
o
n
t
h
s
(
m
o
)
;
A
X
,
A
f
r
i
c
a
n
d
e
r
c
r
o
s
s
(
1
2
A
f
r
i
c
a
n
d
e
r
,
S
h
o
r
t
h
o
r
n
,
H
)
;
A
X
B
X
,
a
n
d
B
X
A
X
,
r
e
c
i
p
r
o
c
a
l
c
r
o
s
s
b
e
t
w
e
e
n
B
X
a
n
d
A
X
;
B
,
B
r
a
h
m
a
n
;
B
v
h
,
B
r
a
u
n
v
i
e
h
;
B
X
,
B
r
a
h
m
a
n
c
r
o
s
s
,
(
1
2
B
r
a
h
m
a
n
,
S
h
o
r
t
h
o
r
n
,
H
)
;
C
,
C
h
a
r
o
l
a
i
s
;
D
r
,
D
r
o
u
g
h
t
m
a
s
t
e
r
;
E
B
V
,
e
s
t
i
m
a
t
e
d
b
r
e
e
d
i
n
g
v
a
l
u
e
;
F
1
C
A
,
r
s
t
c
r
o
s
s
C
h
a
r
o
l
a
i
s
A
n
g
u
s
;
F
1
C
H
,
r
s
t
c
r
o
s
s
C
h
a
r
o
l
a
i
s
H
e
r
e
f
o
r
d
;
F
1
C
S
h
,
r
s
t
c
r
o
s
s
C
h
a
r
o
l
a
i
s
S
h
o
r
t
h
o
r
n
;
F
1
H
A
,
r
s
t
c
r
o
s
s
H
e
r
e
f
o
r
d
A
n
g
u
s
;
F
1
L
A
,
r
s
t
c
r
o
s
s
L
i
m
o
u
s
i
n
A
n
g
u
s
;
F
1
L
H
,
r
s
t
c
r
o
s
s
L
i
m
o
u
s
i
n
H
e
r
e
f
o
r
d
;
F
1
L
S
h
,
r
s
t
c
r
o
s
s
L
i
m
o
u
s
i
n
S
h
o
r
t
h
o
r
n
;
F
1
S
h
S
h
,
r
s
t
c
r
o
s
s
S
h
o
r
t
h
o
r
n
S
h
o
r
t
h
o
r
n
;
F
1
S
i
A
,
r
s
t
c
r
o
s
s
S
i
m
m
e
n
t
a
l
A
n
g
u
s
;
F
1
S
i
H
,
r
s
t
c
r
o
s
s
S
i
m
m
e
n
t
a
l
H
e
r
e
f
o
r
d
;
F
A
,
F
r
e
s
i
a
n
A
n
g
u
s
;
F
H
,
F
r
e
s
i
a
n
H
e
r
e
f
o
r
d
;
G
,
G
e
l
b
v
i
e
h
;
G
A
,
h
i
g
h
g
r
a
d
e
A
f
r
i
c
a
n
d
e
r
;
G
B
,
h
i
g
h
g
r
a
d
e
B
r
a
h
m
a
n
;
H
,
H
e
r
e
f
o
r
d
;
H
A
(
R
)
,
H
e
r
e
f
o
r
d
A
n
g
u
s
(
R
o
t
a
t
i
o
n
-
c
r
o
s
s
h
e
r
d
7
5
%
H
a
n
d
2
5
%
A
)
;
H
A
,
H
e
r
e
f
o
r
d
A
n
g
u
s
;
H
S
h
,
H
e
r
e
f
o
r
d
S
h
o
r
t
h
o
r
n
;
H
x
,
H
e
r
e
f
o
r
d
c
r
o
s
s
;
J
A
,
J
e
r
s
e
y
A
n
g
u
s
;
L
,
L
i
m
o
u
s
i
n
;
l
,
l
i
v
e
a
n
i
m
a
l
m
e
a
s
u
r
e
m
e
n
t
;
M
a
J
A
,
M
a
i
n
e
A
n
j
o
u
(
2
5
%
)
J
e
r
s
e
y
(
2
5
%
)
A
n
g
u
s
(
5
0
%
)
(
t
h
r
e
e
-
b
r
e
e
d
c
o
m
p
o
s
i
t
i
o
n
)
;
M
A
R
C
I
=
B
v
h
L
1
8
H
1
8
A
;
M
A
R
C
I
I
=
S
1
4
H
A
;
M
A
R
C
I
I
I
=
A
;
N
,
N
e
l
o
r
e
;
n
,
s
a
m
p
l
e
n
u
m
b
e
r
;
n
s
,
n
o
t
s
i
g
n
i
c
a
n
t
(
p
>
0
.
0
5
)
;
P
,
P
i
n
z
g
a
u
e
r
;
R
,
R
e
d
P
o
l
l
;
r
g
,
g
e
n
e
t
i
c
c
o
r
r
e
l
a
t
i
o
n
;
r
p
,
p
h
e
n
o
t
y
p
i
c
c
o
r
r
e
l
a
t
i
o
n
;
S
,
s
a
m
p
l
e
t
y
p
e
;
S
C
,
s
c
r
o
t
a
l
c
i
r
c
u
m
f
e
r
e
n
c
e
(
o
r
d
i
a
m
e
t
e
r
)
;
S
D
x
A
,
S
o
u
t
h
D
e
v
o
n
A
n
g
u
s
;
S
i
F
A
,
S
i
m
m
e
n
t
a
l
(
2
5
%
)
F
r
e
s
i
a
n
(
2
5
%
)
A
n
g
u
s
(
5
0
%
)
;
s
m
,
s
e
r
u
m
;
s
p
,
s
p
e
r
m
;
s
p
,
s
p
e
r
m
;
Z
,
Z
e
b
u
;
Z
X
,
z
e
b
u
c
r
o
s
s
.
T
a
b
l
e
3
.
H
e
r
i
t
a
b
i
l
i
t
y
o
f
(
a
)
m
a
l
e
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
a
n
d
(
b
)
f
e
m
a
l
e
r
e
p
r
o
d
u
c
t
i
v
e
p
r
o
g
e
n
y
t
r
a
i
t
s
c
o
r
r
e
l
a
t
e
d
w
i
t
h
s
i
r
e
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
M
a
l
e
F
e
m
a
l
e
T
r
a
i
t
s
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
h
2
C
o
m
m
e
n
t
s
(
a
)
M
a
l
e
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
C
o
r
r
e
c
t
e
d
S
C
B
o
s
t
a
u
r
u
s
C
o
u
l
t
e
r
e
t
a
l
.
(
1
9
7
6
)
C
a
t
t
l
e
;
H
o
6
7
2
m
o
0
.
6
7
0
.
1
0
H
i
g
h
h
2
r
e
l
a
t
i
v
e
t
o
m
a
n
y
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
C
o
n
s
i
s
t
e
n
c
y
o
f
t
e
s
t
e
s
(
T
o
n
o
m
e
t
e
r
r
a
t
i
o
s
)
C
o
u
l
t
e
r
e
t
a
l
.
(
1
9
7
6
)
C
a
t
t
l
e
;
H
o
6
7
2
m
o
0
.
3
4
0
.
1
4
H
i
g
h
h
2
r
e
l
a
t
i
v
e
t
o
m
a
n
y
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
P
r
e
g
n
a
n
c
y
r
a
t
e
l
i
f
e
t
i
m
e
M
a
c
k
i
n
n
o
n
e
t
a
l
.
(
1
9
9
0
a
)
C
a
t
t
l
e
;
H
S
h
A
X
B
X
A
X
B
X
AB
0
.
0
6
0
.
0
8
0
.
1
0
0
.
0
3
0
.
0
2
0
.
1
6
M
e
y
e
r
e
t
a
l
.
(
1
9
9
1
,
1
9
9
0
)
C
a
t
t
l
e
;
A
X
A
X
B
X
0
.
0
0
C
o
r
r
e
c
t
e
d
S
C
M
e
y
e
r
e
t
a
l
.
(
1
9
9
1
,
1
9
9
0
)
C
a
t
t
l
e
;
H
,
A
,
Z
X
1
2
2
4
m
o
0
.
5
7
0
.
4
2
0
.
2
6
D
a
t
a
f
r
o
m
v
a
r
i
o
u
s
s
o
u
r
c
e
s
.
V
a
r
i
a
b
l
e
a
g
e
a
r
o
u
n
d
a
b
o
u
t
p
u
b
e
r
t
y
.
S
o
m
e
o
l
d
e
r
K
o
o
t
s
e
t
a
l
.
(
1
9
9
4
)
C
a
t
t
l
e
Y
e
a
r
l
i
n
g
0
.
4
8
0
.
0
1
9
W
e
i
g
h
t
e
d
,
a
g
e
a
d
j
u
s
t
e
d
C
o
r
r
e
c
t
e
d
S
C
B
o
s
i
n
d
i
c
u
s
M
a
c
k
i
n
n
o
n
e
t
a
l
.
(
1
9
9
1
)
C
a
t
t
l
e
;
Z
X
9
m
o
1
8
m
o
0
.
3
6
0
.
1
2
0
.
2
8
0
.
1
0
B
r
i
n
k
s
(
1
9
9
4
)
;
R
e
v
i
e
w
c
i
t
e
d
d
a
t
a
t
o
1
9
8
9
C
a
t
t
l
e
;
Z
1
2
m
o
0
.
4
9
0
.
0
6
0
.
3
6
0
.
0
6
0
.
4
4
0
.
2
4
0
.
3
8
0
.
1
6
0
.
5
2
0
.
6
8
0
.
4
1
0
.
0
6
0
.
4
0
0
.
0
9
0
.
5
5
0
.
2
1
A
r
e
v
i
e
w
o
f
d
a
t
a
t
o
1
9
8
9
l
i
n
k
i
n
g
1
2
m
o
n
t
h
S
C
t
o
v
a
r
i
o
u
s
p
a
r
a
m
e
t
e
r
s
o
f
g
r
o
w
t
h
a
n
d
r
e
p
r
o
d
u
c
t
i
o
n
V
a
r
g
a
s
e
t
a
l
.
(
1
9
9
8
)
C
a
t
t
l
e
;
B
1
8
m
o
0
.
2
8
n
=
2
8
m
a
l
e
s
n
=
2
6
1
f
e
m
a
l
e
s
M
e
y
e
r
a
n
d
J
o
h
n
s
t
o
n
(
2
0
0
1
)
C
a
t
t
l
e
;
B
1
0
2
6
m
o
0
.
5
0
.
7
M
o
d
e
l
l
e
d
d
a
t
a
o
n
l
y
,
n
o
n
e
o
f
o
r
i
g
i
n
a
l
g
i
v
e
n
E
l
e
r
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
;
N
1
5
m
o
0
.
5
7
0
.
0
3
C
o
r
r
e
c
t
e
d
S
C
B
o
s
t
a
u
r
u
s
T
o
e
l
l
e
a
n
d
R
o
b
i
s
o
n
(
1
9
8
5
)
C
a
t
t
l
e
;
H
6
.
5
m
o
1
2
m
o
0
.
0
8
0
.
2
0
0
.
4
4
0
.
2
4
S
m
i
t
h
e
t
a
l
.
(
1
9
8
9
b
)
C
a
t
t
l
e
;
H
,
A
1
2
m
o
0
.
3
9
A
l
l
o
w
a
n
c
e
s
m
a
d
e
f
o
r
i
n
b
r
e
e
d
i
n
g
o
f
h
e
r
d
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
2
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
m
o
1
1
m
o
1
3
m
o
0
.
5
0
0
.
1
1
0
.
3
3
0
.
1
0
0
.
2
9
0
.
1
0
C
r
o
s
s
-
b
r
e
e
d
i
n
g
e
x
p
e
r
i
m
e
n
t
f
o
l
l
o
w
s
o
n
i
n
l
a
t
e
r
y
e
a
r
s
.
M
u
l
t
i
p
l
e
b
r
e
e
d
s
a
n
d
c
r
o
s
s
e
s
.
n
=
2
3
4
s
i
r
e
g
r
o
u
p
s
o
f
a
b
o
u
t
6
m
a
l
e
s
a
n
d
6
f
e
m
a
l
e
s
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
3
)
C
a
t
t
l
e
;
A
9
1
3
0
.
2
4
0
.
0
8
C
o
n
t
i
n
u
e
d
f
r
o
m
p
r
e
v
i
o
u
s
b
u
t
r
u
n
o
n
s
e
p
a
r
a
t
e
p
r
o
p
e
r
t
y
.
n
=
5
5
0
c
o
w
s
m
a
t
e
d
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
9
1
3
m
o
s
i
t
e
1
s
i
t
e
2
0
.
2
9
0
.
0
7
0
.
3
7
0
.
0
5
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
a
t
2
s
i
t
e
s
.
B
y
n
o
w
h
a
v
e
l
o
n
g
h
i
s
t
o
r
y
o
f
s
e
l
e
c
t
i
o
n
e
c
t
s
E
v
a
n
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
1
2
m
o
0
.
7
1
0
.
1
3
0
.
7
8
0
.
1
6
n
=
1
2
2
0
b
u
l
l
s
.
P
r
e
g
n
a
n
c
y
a
s
y
e
s
o
r
n
o
.
S
e
c
o
n
d
h
2
e
s
t
i
m
a
t
e
s
a
n
d
c
o
r
r
e
l
a
t
i
o
n
f
r
o
m
m
u
l
t
i
v
a
r
i
a
t
e
a
n
a
l
y
s
i
s
T
a
b
l
e
3
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
F
e
m
a
l
e
T
r
a
i
t
s
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
h
2
C
o
m
m
e
n
t
s
M
w
a
n
s
a
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
H
,
A
1
2
m
o
0
.
6
4
M
a
r
t
i
n
e
z
-
V
e
l
a
z
q
u
e
z
e
t
a
l
.
(
2
0
0
3
)
C
a
t
t
l
e
;
H
,
A
,
H
A
(
R
)
,
L
,
S
,
C
,
P
,
G
,
B
v
h
,
M
A
R
C
I
,
I
I
&
I
I
I
1
2
m
o
0
.
4
1
0
.
0
4
n
>
7
0
0
0
T
e
s
t
i
c
u
l
a
r
v
o
l
u
m
e
T
o
e
l
l
e
a
n
d
R
o
b
i
s
o
n
(
1
9
8
5
)
C
a
t
t
l
e
;
H
6
.
5
m
o
1
2
m
o
0
.
3
4
0
.
1
4
0
.
2
1
0
.
1
2
G
n
R
H
-
s
t
i
m
u
l
a
t
e
d
t
e
s
t
o
s
t
e
r
o
n
e
M
a
c
k
i
n
n
o
n
e
t
a
l
.
(
1
9
9
1
)
C
a
t
t
l
e
;
Z
X
9
m
o
1
8
m
o
0
.
4
2
0
.
2
8
0
.
5
5
0
.
4
2
G
n
R
H
-
s
t
i
m
u
l
a
t
e
d
L
H
H
a
l
e
y
e
t
a
l
.
(
1
9
8
9
)
S
h
e
e
p
2
.
5
5
m
o
0
.
4
4
0
.
0
2
I
G
F
-
1
Y
i
l
m
a
z
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
;
A
5
6
m
o
6
8
m
o
0
.
4
3
0
.
0
8
0
.
4
1
0
.
0
8
S
e
l
e
c
t
i
o
n
o
f
h
i
g
h
a
n
d
l
o
w
l
i
n
e
s
s
t
a
r
t
e
d
1
9
8
9
1
9
9
0
a
n
d
i
n
b
r
e
e
d
i
n
g
c
o
n
t
i
n
u
e
d
w
i
t
h
n
=
8
b
u
l
l
s
p
e
r
y
e
a
r
a
n
d
n
=
1
0
0
c
o
w
s
p
e
r
y
e
a
r
(
b
)
F
e
m
a
l
e
r
e
p
r
o
d
u
c
t
i
v
e
p
r
o
g
e
n
y
t
r
a
i
t
s
c
o
r
r
e
l
a
t
e
d
w
i
t
h
s
i
r
e
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
A
g
e
p
u
b
e
r
t
y
S
m
i
t
h
e
t
a
l
.
(
1
9
8
9
a
)
C
a
t
t
l
e
;
H
,
A
0
.
1
0
0
.
1
7
V
a
r
g
a
s
e
t
a
l
.
(
1
9
9
8
)
C
a
t
t
l
e
;
B
0
.
4
2
n
=
2
8
#
n
=
2
6
1
$
S
p
l
a
n
e
t
a
l
.
(
1
9
9
8
)
C
a
t
t
l
e
0
.
4
7
0
.
0
7
M
a
r
t
i
n
e
z
-
V
e
l
a
z
q
u
e
z
e
t
a
l
.
(
2
0
0
3
)
C
a
t
t
l
e
;
H
,
A
,
H
,
A
(
R
)
,
L
,
S
,
C
,
P
,
G
,
B
v
h
,
M
A
R
C
I
,
I
I
&
I
I
I
0
.
1
6
0
.
0
4
n
>
7
0
0
0
S
t
a
n
d
a
r
d
i
z
e
d
a
g
e
1
s
t
o
e
s
t
r
u
s
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
2
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
0
.
3
2
0
.
1
0
C
r
o
s
s
-
b
r
e
e
d
i
n
g
e
x
p
e
r
i
m
e
n
t
f
o
l
l
o
w
s
o
n
i
n
l
a
t
e
r
y
e
a
r
s
.
M
u
l
t
i
p
l
e
b
r
e
e
d
s
a
n
d
c
r
o
s
s
e
s
.
n
=
2
3
4
s
i
r
e
g
r
o
u
p
s
o
f
a
b
o
u
t
6
m
a
l
e
s
a
n
d
6
f
e
m
a
l
e
s
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
3
)
C
a
t
t
l
e
;
A
0
.
2
3
0
.
1
0
C
o
n
t
i
n
u
e
d
f
r
o
m
p
r
e
v
i
o
u
s
b
u
t
r
u
n
o
n
s
e
p
a
r
a
t
e
p
r
o
p
e
r
t
y
.
n
=
5
5
0
c
o
w
s
m
a
t
e
d
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
S
i
t
e
1
0
.
3
2
0
.
1
0
S
i
t
e
2
0
.
3
0
0
.
0
5
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
a
t
2
s
i
t
e
s
.
B
y
n
o
w
h
a
v
e
l
o
n
g
h
i
s
t
o
r
y
o
f
s
e
l
e
c
t
i
o
n
e
c
t
s
A
g
e
a
t
1
s
t
c
a
l
f
S
m
i
t
h
e
t
a
l
.
(
1
9
8
9
a
)
C
a
t
t
l
e
;
H
,
A
0
.
0
1
0
.
1
2
K
o
o
t
s
e
t
a
l
.
(
1
9
9
4
)
C
a
t
t
l
e
0
.
0
6
0
.
0
2
W
e
i
g
h
t
e
d
M
a
r
t
i
n
e
z
-
V
e
l
a
z
q
u
e
z
e
t
a
l
.
(
2
0
0
3
)
C
a
t
t
l
e
;
H
,
A
,
H
A
(
R
)
,
L
,
S
,
C
,
P
,
G
,
B
v
h
,
M
A
R
C
I
,
I
I
&
I
I
I
0
.
0
8
0
.
0
4
n
>
7
0
0
0
C
a
l
v
i
n
g
d
a
t
e
S
m
i
t
h
e
t
a
l
.
(
1
9
8
9
a
)
C
a
t
t
l
e
;
H
,
A
0
.
0
9
0
.
1
3
K
o
o
t
s
e
t
a
l
.
(
1
9
9
4
)
C
a
t
t
l
e
0
.
0
8
0
.
0
1
4
W
e
i
g
h
t
e
d
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
S
i
t
e
1
0
.
0
4
0
.
0
9
S
i
t
e
2
0
.
0
9
0
.
0
4
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
a
t
2
s
i
t
e
s
.
B
y
n
o
w
h
a
v
e
l
o
n
g
h
i
s
t
o
r
y
o
f
s
e
l
e
c
t
i
o
n
e
c
t
s
P
r
e
g
n
a
n
c
y
r
a
t
e
a
s
y
e
a
r
l
i
n
g
M
o
r
r
i
s
a
n
d
C
u
l
l
e
n
(
1
9
9
4
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
0
.
0
4
0
.
0
4
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
s
t
u
d
i
e
s
.
N
e
w
s
i
t
e
.
H
,
A
a
n
d
o
t
h
e
r
b
r
e
e
d
s
K
o
o
t
s
e
t
a
l
.
(
1
9
9
4
)
C
a
t
t
l
e
0
.
0
5
0
.
0
1
W
e
i
g
h
t
e
d
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
S
i
t
e
1
0
.
0
4
0
.
0
4
S
i
t
e
2
0
.
1
2
0
.
0
5
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
a
t
2
s
i
t
e
s
.
B
y
n
o
w
h
a
v
e
l
o
n
g
h
i
s
t
o
r
y
o
f
s
e
l
e
c
t
i
o
n
e
c
t
s
E
v
a
n
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
0
.
1
4
0
.
0
9
0
.
2
4
0
.
1
2
n
=
1
2
2
0
b
u
l
l
s
,
p
r
e
g
n
a
n
c
y
a
s
y
e
s
o
r
n
o
.
S
e
c
o
n
d
h
2
e
s
t
i
m
a
t
e
s
f
r
o
m
m
u
l
t
i
v
a
r
i
a
t
e
a
n
a
l
y
s
i
s
E
l
e
r
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
;
N
G
r
o
u
p
1
0
.
6
9
0
.
0
9
G
r
o
u
p
2
0
.
6
3
0
.
0
8
O
v
u
l
a
t
i
o
n
r
a
t
e
C
u
n
n
i
n
g
h
a
m
e
t
a
l
.
(
1
9
7
9
)
P
i
g
0
.
4
2
0
.
0
6
output (Killian et al. 1993; Cancel et al. 1997; Brandon
et al. 1999; Roudebush and Diehl 2001; Brackett et al.
2004; Moura et al. 2006). However, one must consider
that each protein factor, although important, is simply
one of many involved in the complex process of
fertilization. This suggests that subfertility is a multifac-
torial problem. Holroyd et al. (2002) recommended the
use of a multi-level statistical analysis to create a model
containing a group of factors which best explains the
dierences in fertility between bulls. Further, there is
evidence in Table 1 that a combined index based on
multiple proteins factors (osteopontin and spermadhe-
sin, seminal plasma proteins BSP30 and phospholipase
A
2
), as measured using seminal protein electrophoresis,
may provide a general and highly correlated measure of
fertility (Killian et al. 1993; Moura et al. 2006). Osteo-
pontin is one of these index proteins found in seminal
plasma, and the relative amount of this protein has been
correlated with fertility in dairy bulls (Killian et al. 1993;
Cancel et al. 1997; Moura et al. 2006). This protein has
also been shown to be secreted by the epithelial cells in
the bovine oviduct and to stimulate fertilization and
embryo development (Cancel et al. 1997).
The only potential specic adaptive trait that was
identied in this review involved 11b-hydroxysteroid
dehydrogenase (11bHSD). In a review of glucocorticoid
metabolism and reproduction in a number of mamma-
lian species, Michael et al. (2003) reported that this
enzyme catalyses the reversible inactivation of cortisol
and corticosterone to their inert 11-ketosteroid metab-
olites, cortisone and 11-dehydroxycorticosterone. Fur-
ther, studies in rodents have shown that reduced
expression or activity of 11b-HSD1 in testis Leydig
cells allows physiological concentrations of glucocortic-
oids to inhibit testosterone biosynthesis, resulting in a
disturbance in spermatogenesis (Michael et al. 2003).
11bHSD has also been detected in the seminal plasma of
dairy bulls (A. E. Michael, pers. comm.), and it may
play a physiological role in maintaining semen quality.
The focus of this review is not to simply predict male
fertility but to enhance the fertility of the herd by
selecting traits that improve the fertility of both male
and female progeny. Table 2 lists the male reproductive
traits that have been reported to be associated with
female fertility. Bovine pre-pubertal scrotal circumfer-
ence and its association with pre-pubertal female prog-
eny traits (age of puberty Brinks et al. 1978; King
et al. 1983; Vargas et al. 1998; Martinez-Velazquez et al.
2003; standardized age at rst oestrus Morris et al.
1992, 1993, 1999; age at rst calf Smith et al. 1989b;
days to calving Meyer et al. 1991; Morris et al. 1999;
Meyer and Johnston 2001; yearling pregnancy rate
Morris and Cullen 1994; Eler et al. 2004; heifer
pregnancy rate Evans et al. 1999; lifetime pregnancy
rate Toelle and Robison 1985; Morris and Cullen
1994; Morris et al. 1999; Mwansa et al. 2000; lifetime
calf production Morris and Cullen 1994; and an
estimated breeding value (EBV) for fertility Bamualim
et al. 1984) make up the bulk of the data available in
the literature, and it has been included for reference
(Table 2). Other data for pre-pubertal male traits are
sparse. The GnRH-stimulated LH response oers
promise (Haley et al. 1989), and IGF-1 shows some T
a
b
l
e
3
.
(
C
o
n
t
i
n
u
e
d
)
M
a
l
e
F
e
m
a
l
e
T
r
a
i
t
s
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
A
g
e
h
2
C
o
m
m
e
n
t
s
M
o
r
r
i
s
a
n
d
C
u
l
l
e
n
(
1
9
9
4
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
0
.
0
4
0
.
0
7
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
s
t
u
d
i
e
s
.
N
e
w
s
i
t
e
.
M
u
l
t
i
p
l
e
b
r
e
e
d
s
a
n
d
c
r
o
s
s
e
s
K
o
o
t
s
e
t
a
l
.
(
1
9
9
4
)
C
a
t
t
l
e
0
.
1
7
0
.
0
1
5
W
e
i
g
h
t
e
d
M
o
r
r
i
s
e
t
a
l
.
(
1
9
9
9
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
S
i
t
e
1
0
.
0
4
0
.
0
7
S
i
t
e
2
0
.
0
4
0
.
0
5
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
a
t
2
s
i
t
e
s
.
B
y
n
o
w
h
a
v
e
l
o
n
g
h
i
s
t
o
r
y
o
f
s
e
l
e
c
t
i
o
n
e
c
t
s
T
o
e
l
l
e
a
n
d
R
o
b
i
s
o
n
(
1
9
8
5
)
C
a
t
t
l
e
;
H
0
.
0
6
0
.
0
6
M
w
a
n
s
a
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
F
1
H
A
,
F
1
C
H
,
F
1
C
A
,
F
1
C
S
h
,
F
1
S
i
H
,
F
1
S
i
A
,
F
1
S
i
S
h
,
F
1
L
H
,
F
1
L
A
,
F
1
L
S
h
0
.
1
6
C
a
l
v
i
n
g
r
a
t
e
l
i
f
e
t
i
m
e
M
o
r
r
i
s
a
n
d
C
u
l
l
e
n
(
1
9
9
4
)
C
a
t
t
l
e
;
H
,
A
,
H
A
,
H
A
(
R
)
,
S
D
x
A
,
J
A
,
M
a
J
A
,
F
A
,
S
i
F
A
,
F
H
0
.
0
4
0
.
0
9
C
o
n
t
i
n
u
a
t
i
o
n
o
f
p
r
e
v
i
o
u
s
s
t
u
d
i
e
s
.
N
e
w
s
i
t
e
.
M
u
l
t
i
p
l
e
b
r
e
e
d
s
a
n
d
c
r
o
s
s
e
s
K
o
o
t
s
e
t
a
l
.
(
1
9
9
4
)
C
a
t
t
l
e
0
.
1
7
0
.
0
1
W
e
i
g
h
t
e
d
O
N
e
i
l
l
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
;
B
0
.
0
7
0
.
0
3
5
A
,
A
n
g
u
s
;
A
g
e
,
a
g
e
o
f
s
a
m
p
l
i
n
g
i
n
m
o
n
t
h
s
(
m
o
)
;
A
X
,
A
f
r
i
c
a
n
d
e
r
c
r
o
s
s
(
1
2
A
f
r
i
c
a
n
d
e
r
,
S
h
o
r
t
h
o
r
n
,
H
)
;
A
X
B
X
,
r
e
c
i
p
r
o
c
a
l
c
r
o
s
s
b
e
t
w
e
e
n
B
X
a
n
d
A
X
;
B
,
B
r
a
h
m
a
n
;
B
v
h
,
B
r
a
u
n
v
i
e
h
;
B
X
,
B
r
a
h
m
a
n
c
r
o
s
s
,
(
1
2
B
r
a
h
m
a
n
,
S
h
o
r
t
h
o
r
n
,
H
)
;
C
,
C
h
a
r
o
l
a
i
s
;
F
1
C
A
,
r
s
t
c
r
o
s
s
C
h
a
r
o
l
a
i
s
A
n
g
u
s
;
F
1
C
H
,
r
s
t
c
r
o
s
s
C
h
a
r
o
l
a
i
s
H
e
r
e
f
o
r
d
;
F
1
C
S
h
,
r
s
t
c
r
o
s
s
C
h
a
r
o
l
a
i
s
S
h
o
r
t
h
o
r
n
;
F
1
H
A
,
r
s
t
c
r
o
s
s
H
e
r
e
f
o
r
d
A
n
g
u
s
;
F
1
L
A
,
r
s
t
c
r
o
s
s
L
i
m
o
u
s
i
n
A
n
g
u
s
;
F
1
L
H
,
r
s
t
c
r
o
s
s
L
i
m
o
u
s
i
n
H
e
r
e
f
o
r
d
;
F
1
L
S
h
,
r
s
t
c
r
o
s
s
L
i
m
o
u
s
i
n
S
h
o
r
t
h
o
r
n
;
F
1
S
h
S
h
,
r
s
t
c
r
o
s
s
S
h
o
r
t
h
o
r
n
S
h
o
r
t
h
o
r
n
;
F
1
S
i
A
,
r
s
t
c
r
o
s
s
S
i
m
m
e
n
t
a
l
A
n
g
u
s
;
F
1
S
i
H
,
r
s
t
c
r
o
s
s
S
i
m
m
e
n
t
a
l
H
e
r
e
f
o
r
d
;
F
A
,
F
r
e
s
i
a
n
A
n
g
u
s
;
F
H
,
F
r
e
s
i
a
n
H
e
r
e
f
o
r
d
;
G
,
G
e
l
b
v
i
e
h
;
H
,
H
e
r
e
f
o
r
d
;
h
2
,
h
e
r
i
t
a
b
i
l
i
t
y
;
H
A
(
R
)
,
H
e
r
e
f
o
r
d
A
n
g
u
s
(
R
o
t
a
t
i
o
n
-
c
r
o
s
s
h
e
r
d
7
5
%
H
a
n
d
2
5
%
A
)
;
H
A
,
H
e
r
e
f
o
r
d
A
n
g
u
s
;
H
o
,
H
o
l
s
t
e
i
n
;
H
S
h
,
H
e
r
e
f
o
r
d
S
h
o
r
t
h
o
r
n
;
J
A
,
J
e
r
s
e
y
A
n
g
u
s
;
L
,
L
i
m
o
u
s
i
n
;
M
a
J
A
,
M
a
i
n
e
A
n
j
o
u
(
2
5
%
)
J
e
r
s
e
y
(
2
5
%
)
A
n
g
u
s
(
5
0
%
)
(
t
h
r
e
e
-
b
r
e
e
d
c
o
m
p
o
s
i
t
i
o
n
)
;
M
A
R
C
I
=
B
v
h
L
1
8
H
1
8
A
;
M
A
R
C
I
I
=
S
1
4
H
A
;
M
A
R
C
I
I
I
=
A
;
N
,
N
e
l
o
r
e
;
n
,
s
a
m
p
l
e
n
u
m
b
e
r
;
P
,
P
i
n
z
g
a
u
e
r
;
R
,
R
e
d
P
o
l
l
;
S
C
,
s
c
r
o
t
a
l
c
i
r
c
u
m
f
e
r
e
n
c
e
(
o
r
d
i
a
m
e
t
e
r
)
;
S
D
x
A
,
S
o
u
t
h
D
e
v
o
n
A
n
g
u
s
;
S
i
F
A
,
S
i
m
m
e
n
t
a
l
(
2
5
%
)
F
r
e
s
i
a
n
(
2
5
%
)
A
n
g
u
s
(
5
0
%
)
;
Z
,
Z
e
b
u
;
Z
X
,
z
e
b
u
c
r
o
s
s
.
T
a
b
l
e
4
.
G
e
n
e
t
i
c
m
a
r
k
e
r
s
o
f
m
a
l
e
r
e
p
r
o
d
u
c
t
i
v
e
t
r
a
i
t
s
w
i
t
h
e
e
c
t
s
o
n
f
e
m
a
l
e
p
r
o
g
e
n
y
M
a
l
e
g
e
n
e
t
i
c
m
a
r
k
e
r
R
e
f
e
r
e
n
c
e
S
p
e
c
i
e
s
B
r
e
e
d
M
a
l
e
t
r
a
i
t
F
e
m
a
l
e
p
r
o
g
e
n
y
c
o
r
r
e
l
a
t
e
d
t
r
a
i
t
s
C
o
m
m
e
n
t
s
R
A
P
D
M
a
r
k
e
r
s
A
l
v
e
s
e
t
a
l
.
(
2
0
0
5
)
C
a
t
t
l
e
;
N
E
a
r
l
y
p
u
b
e
r
t
y
n
=
3
4
,
m
a
l
e
o
n
l
y
,
m
a
r
k
e
r
s
l
i
n
k
e
d
t
o
e
a
r
l
y
o
r
l
a
t
e
g
r
o
u
p
b
u
t
n
o
t
u
s
e
d
f
o
r
p
r
e
d
i
c
t
i
o
n
s
Q
T
L
c
h
r
o
m
o
s
o
m
e
5
C
a
s
a
s
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
H
i
g
h
F
S
H
H
i
g
h
F
S
H
o
v
u
l
a
t
i
o
n
r
a
t
e
L
a
r
g
e
e
e
c
t
s
b
u
t
b
a
s
e
d
o
n
b
r
e
e
d
d
i
e
r
e
n
c
e
s
(
i
.
e
.
j
u
s
t
u
s
e
t
h
e
b
r
e
e
d
s
)
K
a
p
p
e
s
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
F
o
l
l
i
c
u
l
a
r
r
e
c
r
u
i
t
m
e
n
t
L
i
e
n
e
t
a
l
.
(
2
0
0
0
)
C
a
t
t
l
e
T
w
i
n
n
i
n
g
i
n
p
r
o
g
e
n
y
P
o
l
y
m
o
r
p
h
i
s
m
I
G
F
-
1
T
w
i
n
n
i
n
g
N
o
r
w
e
g
i
a
n
c
a
t
t
l
e
C
r
u
i
c
k
s
h
a
n
k
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
T
w
i
n
n
i
n
g
Q
T
L
c
h
r
o
m
o
s
o
m
e
1
0
N
o
n
n
e
m
a
n
a
n
d
R
o
h
r
e
r
(
2
0
0
3
)
P
i
g
A
g
e
p
u
b
e
r
t
y
o
v
u
l
a
t
i
o
n
r
a
t
e
N
i
p
p
l
e
n
u
m
b
e
r
F
S
H
P
o
r
c
i
n
e
c
h
r
o
m
o
s
o
m
e
1
0
h
a
r
b
o
u
r
s
s
e
v
e
r
a
l
Q
T
L
f
o
r
r
e
p
r
o
d
u
c
t
i
o
n
t
r
a
i
t
s
Q
T
L
o
n
c
h
r
o
m
o
s
o
m
e
1
4
Q
T
L
a
l
s
o
o
n
c
h
r
o
m
o
s
o
m
e
s
1
7
,
5
,
1
8
,
1
,
6
,
4
,
1
1
,
2
1
,
2
2
,
2
5
,
3
,
1
2
,
2
4
,
1
0
,
2
0
G
o
n
d
a
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
O
v
u
l
a
t
i
o
n
r
a
t
e
a
n
d
t
w
i
n
n
i
n
g
r
a
t
e
P
o
t
e
n
t
i
a
l
t
o
i
n
c
r
e
a
s
e
r
e
p
r
o
d
u
c
t
i
o
n
e
c
i
e
n
c
y
i
n
c
a
t
t
l
e
t
h
r
o
u
g
h
t
w
i
n
n
i
n
g
.
T
w
i
n
n
i
n
g
r
a
t
e
i
s
a
p
r
o
d
u
c
t
o
f
o
v
u
l
a
t
i
o
n
r
a
t
e
,
c
o
n
c
e
p
t
i
o
n
r
a
t
e
a
n
d
e
m
b
r
y
o
s
u
r
v
i
v
a
l
Q
T
L
c
h
r
o
m
o
s
o
m
e
2
9
C
a
s
a
s
e
t
a
l
.
(
2
0
0
4
)
C
a
t
t
l
e
t
e
s
t
e
s
w
t
t
e
s
t
e
s
v
o
l
u
m
e
b
o
d
y
w
t
a
g
e
p
u
b
e
r
t
y
a
g
e
p
u
b
e
r
t
y
L
a
r
g
e
e
e
c
t
s
b
u
t
b
a
s
e
d
o
n
b
r
e
e
d
d
i
e
r
e
n
c
e
s
(
i
.
e
.
j
u
s
t
u
s
e
t
h
e
b
r
e
e
d
s
)
M
a
p
p
e
d
g
e
n
e
s
R
o
n
c
o
l
l
e
t
a
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
P
r
o
t
e
i
n
p
o
t
e
n
t
i
a
t
e
s
t
h
e
c
a
p
a
c
i
t
a
t
i
o
n
o
f
b
o
v
i
n
e
e
p
i
d
i
d
y
m
a
l
s
p
e
r
m
i
n
d
u
c
e
d
b
y
h
e
p
a
r
i
n
a
n
d
h
i
g
h
d
e
n
s
i
t
y
l
i
p
o
p
r
o
t
e
i
n
s
(
H
D
L
)
G
e
n
o
m
e
m
a
p
p
i
n
g
o
f
B
S
P
A
3
(
b
o
v
i
n
e
s
e
m
i
n
a
l
p
l
a
s
m
a
p
r
o
t
e
i
n
A
3
)
.
S
e
c
r
e
t
o
r
y
p
r
o
d
u
c
t
o
f
s
e
m
i
n
a
l
v
e
s
i
c
l
e
s
.
M
u
l
t
i
p
l
e
b
i
n
d
i
n
g
a
n
d
f
u
n
c
t
i
o
n
a
l
p
r
o
p
e
r
t
i
e
s
J
a
c
o
b
s
e
t
a
l
.
(
2
0
0
2
)
C
a
t
t
l
e
F
A
B
G
L
(
1
7
b
-
h
y
d
r
o
x
y
s
t
e
r
o
i
d
d
e
h
y
d
r
o
g
e
n
a
s
e
)
g
e
n
e
i
s
a
c
a
n
d
i
d
a
t
e
g
e
n
e
f
o
r
r
e
p
r
o
d
u
c
t
i
o
n
t
r
a
i
t
s
i
n
p
i
g
s
a
-
A
c
t
i
n
i
n
g
e
n
e
(
A
C
T
N
1
)
W
i
m
m
e
r
s
e
t
a
l
.
(
2
0
0
5
)
P
i
g
A
C
T
N
1
a
s
s
o
c
i
a
t
e
d
w
i
t
h
N
R
R
e
c
t
o
f
p
o
l
y
m
o
r
p
h
G
G
0
.
4
9
A
A
)
4
.
9
0
N
u
m
b
e
r
o
f
p
i
g
l
e
t
s
b
o
r
n
a
l
i
v
e
(
N
B
A
)
G
G
0
.
0
7
A
A
)
1
.
0
1
G
f
r
e
q
u
e
n
c
y
0
.
7
5
A
f
r
e
q
u
e
n
c
y
0
.
2
5
c
-
A
c
t
i
n
g
e
n
e
(
A
C
T
G
2
)
W
i
m
m
e
r
s
e
t
a
l
.
(
2
0
0
5
)
P
i
g
A
C
T
N
2
a
s
s
o
c
i
a
t
e
d
w
i
t
h
S
e
m
e
n
v
o
l
u
m
e
i
n
p
u
r
e
b
r
e
d
b
o
a
r
s
E
e
c
t
r
a
n
g
e
)
1
6
t
o
+
3
S
p
e
r
m
m
o
t
i
l
i
t
y
i
n
c
r
o
s
s
-
b
r
e
d
b
o
a
r
s
E
e
c
t
r
a
n
g
e
)
0
.
3
t
o
+
1
.
3
1
2
a
l
l
e
l
e
s
,
5
w
i
t
h
>
5
%
f
r
e
q
u
e
n
c
y
F
S
H
,
f
o
l
l
i
c
l
e
-
s
t
i
m
u
l
a
t
i
n
g
h
o
r
m
o
n
e
;
G
a
n
d
A
a
r
e
t
h
e
a
l
l
e
l
e
s
a
s
s
o
c
i
a
t
e
d
w
i
t
h
t
h
e
A
C
T
N
1
l
o
c
u
s
a
n
d
G
G
a
n
d
A
A
r
e
p
r
e
s
e
n
t
t
h
e
h
o
m
o
z
y
g
o
u
s
g
e
n
o
t
y
p
e
s
a
t
t
h
i
s
l
o
c
u
s
;
I
G
F
-
1
,
I
n
s
u
l
i
n
-
l
i
k
e
g
r
o
w
t
h
f
a
c
t
o
r
1
;
n
,
s
a
m
p
l
e
n
u
m
b
e
r
;
N
R
R
,
n
o
n
-
r
e
t
u
r
n
r
a
t
e
;
Q
T
L
,
q
u
a
n
t
i
t
a
t
i
v
e
t
r
a
i
t
l
o
c
i
;
R
A
P
D
,
R
a
n
d
o
m
A
m
p
l
i
e
d
P
o
l
y
m
o
r
p
h
i
c
D
N
A
m
a
r
k
e
r
s
a
r
e
D
N
A
f
r
a
g
m
e
n
t
s
f
r
o
m
p
o
l
y
m
e
r
a
s
e
c
h
a
i
n
r
e
a
c
t
i
o
n
(
P
C
R
)
a
m
p
l
i
c
a
t
i
o
n
o
f
r
a
n
d
o
m
s
e
g
m
e
n
t
s
o
f
g
e
n
o
m
i
c
D
N
A
w
i
t
h
s
i
n
g
l
e
p
r
i
m
e
r
o
f
a
r
b
i
t
r
a
r
y
n
u
c
l
e
o
t
i
d
e
s
e
q
u
e
n
c
e
.
correlations with reproductive traits (Gong et al. 1991;
Yilmaz et al. 2004). There are even less data for the
post-pubertal male traits (Table 2). Therefore, because
of the lack of direct data, we must speculate, based on
known mechanisms in female reproduction, as to which
male traits may be linked to important female repro-
ductive traits.
To achieve satisfactory genetic progress based on
selection for male reproductive traits, these traits must be
moderately heritable. Moreover, if the male traits are to
be linked to improvement in female reproduction, the
linked female traits must be favourably correlated with
the male traits of interest. Table 3 provides a list of the
heritabilities of various male and female reproductive
traits. In general, those traits that are close measures of
innate fertility are moderately heritable while traits that
are principally measures of expressed fertility are not
heritable. Thus, the measures of calf-getting ability or
pregnancy rate for both male (Mackinnon et al. 1990a;
Meyer et al. 1990, 1991) and female cattle (Toelle and
Robison 1985; Mackinnon et al. 1990a; Koots et al.
1994; Morris and Cullen 1994; Evans et al. 1999; Morris
et al. 1999; Mwansa et al. 2000; ONeill et al. 2000; Eler
et al. 2004) have either a low heritability or are not
heritable. In contrast, scrotal circumference (Coulter
et al. 1976; Toelle and Robison 1985; Smith et al. 1989b;
Meyer et al. 1990, 1991; Mackinnon et al. 1991; Morris
et al. 1992, 1999; Brinks 1994; Koots et al. 1994; Vargas
et al. 1998; Evans et al. 1999; Mwansa et al. 2000; Meyer
and Johnston 2001; Martinez-Velazquez et al. 2003; Eler
et al. 2004), tone of testes (Coulter et al. 1976) and age of
puberty (Splan et al. 1998; Vargas et al. 1998) are
moderately heritable. Further, increased sperm produc-
tion from genetically superior sperm donors has the
potential for increasing the number of progeny from
these sires derived by articial insemination. Coulter and
Foote (1979) reported that while bull management and
seminal collection practices have improved sperm har-
vest, little attention has been given to testicular evalua-
tion and selection as a mechanism for increasing the
quantity and quality of spermatozoa produced from
genetically superior sires. While data are scarce, moder-
ate heritability estimates have been reported for GnRH-
stimulated LH (Haley et al. 1989; Mackinnon et al.
1991) and IGF-1 (Yilmaz et al. 2004) (Table 3).
The previous discussion has focused on the identi-
cation of a number of traits in both male and female
animals that inuence either male or female fertility, or
on male traits that are genetically correlated to female
fertility traits. These male and female reproductive traits
range from not being heritable to being low to moder-
ately heritable. However, some of these fertility traits,
while genetically determined traits, are dicult to
evaluate and therefore dicult to improve by selection.
Another strategy that can assist in the improvement of
economically important male and female fertility traits is
the mapping of genes. This strategy oers the possibility
of marker-assisted selection (MAS), which is expected to
improve genetic response by enhancing both the accu-
racy and the timing of selection (Soller and Beckman
1982; Smith and Simpson 1986). Further, the detection of
genes inuencing quantitative traits such as fertility traits
is now feasible with the availability of a large number of
genetic markers covering the genomes of dierent species
(cattle Fries et al. 1989; Georges et al. 1990; Barendse
et al. 1994 and Bishop et al. 1994; sheep Crawford
et al. 1994; and pigs Rohrer et al. 1994).
Table 4 lists some examples of known genetic markers
and mapped genes with associations with both male and
female reproductive performance. Two of the major
factors that inuence the reproduction eciency of a
cattle herd are age at puberty and post-partum anoes-
trus interval (Cundi et al. 1992). Therefore, an oppor-
tunity exists to evaluate genetic markers associated with
these factors and include the genetic markers for age at
puberty in cattle (Casas et al. 2004; Alves et al. 2005),
and the genetic markers associated with quantitative
trait loci (QTL) for follicular recruitment (Kappes et al.
2000) and ovulation ovulation rate (Casas et al. 2004).
In addition, the mapped genes reported to be associated
with bovine seminal plasma protein A3 (Roncolleta
et al. 2002) and 17b-hydroxysteroid dehydrogenase
associated with testosterone production (Jacobs et al.
2002) warrant further investigation. Finally, a number
of genetic markers and genes associated with male and
female reproductive traits were also identied in the pig
(Nonneman and Rohrer 2003; Wimmers et al. 2005).
These genetic markers and genes could be evaluated in
cattle at a later date.
Conclusions
As shown in Tables 14, data relevant to the objective of
this review of identifying male traits potentially genet-
ically correlated with female fertility traits, with partic-
ular emphasis on identifying traits which could be
assessed in pre-pubertal bulls, are scarce. This situation
exists despite this issue being of concern to the cattle
industry for many years. Therefore, the way ahead must
be heavily based on an understanding of the physiolog-
ical mechanisms controlling fertility in males and
females rather than on published data dening the
relationship between phenotypic traits and fertility.
Specic conclusions of the review and recommenda-
tions for further study are as follows:
1. Testicular development. The measurement of scrotal
circumference is still the best method of assessing
testicular development, but some ne tuning in the
form of use of the Barth tape (Barth 2000), which may
improve reproducibility, could be considered. Under
more extensive research conditions and where large
numbers of bulls are to be measured, we recommend
that scrotal circumference should be measured at
weaning (6 months of age), 9, 12, 15, 18, 21 and
24 months of age to monitor scrotal development and
assess at what age it may rst be associated with
female fertility.
2. Endocrine control. Endocrine control will always
be dicult to evaluate practically. However, endo-
crine control is fundamental to normal function in
both the male and female, and there are periods of
critical development of the hypothalamicpituitary
gonadal axis. In particular, these occur prior to
puberty, after parturition and also from dry season
(MayOctober) to wet (NovemberApril) season
(Anonymous 1986) in bulls in northern Australia.
Thus, there is a need to identify some means of
evaluating this component of fertility. Limited data
demonstrate that GnRH-stimulated serum LH con-
centrations in pre-pubertal bull calves are predictive
of testes development and function, are associated
with reproductive function in ovine female progeny
and are moderately heritable in tropically adapted
bulls and dairy females. Based on evidence of pheno-
typic and genetic correlations from this systematic
review and this indicator trait meeting all established
criteria, further assessment of GnRH-stimulated
serum LH concentrations in pre-pubertal bulls as an
early-life predictor of fertility is recommended. The-
oretical considerations based on available knowledge
suggest that pre-pubertal inhibin measurement could
provide an indication of hypothalamicpituitary
gonadal axis development similar to the GnRH-
stimulated LH measurement. As inhibin measurement
simply requires an additional blood sample collection
at 35 months of age, an immunoassay of the sample
is recommended for investigation.
3. Spermatogenesis. Per cent morphologically normal
sperm and the spermiogram are still the best practical
measures of the quality of spermatozoa in ejaculates,
and given that they have been consistently shown to
be signicantly related to bull fertility (Fitzpatrick
et al. 2002), further investigation to determine the
relationship with female fertility is recommended.
Recommended ages for assessment of sperm quality
include 12, 18 and 24 months of age. Further, it is
important that the profound inuences of body
weight, diet, environmental and iatrogenic inuences
be considered in the interpretation of the spermio-
gram.
4. Seminal plasma proteins. A large number of seminal
plasma proteins and factors linked to the fertilizing
potential of morphologically normal, motile sperm
have been identied, and several have been correlated
with fertility in livestock. As these proteins factors
may play an important role in fertilization and early
embryo development, independently of sperm mor-
phology, we recommend that seminal plasma samples
from bulls be collected in testing programmes for a
selection of these proteins factors based on the
ndings in Table 1. Seminal proteins linked to male
reproductive function, which have been identied,
include spermadhesin, osteopontin, bovine seminal
protein 30 kDa and phospholipase A
2
. Other proteins
may be identied as correlations with components of
fertility are made. Based on results from this system-
atic review and this indicator trait meeting all
established criteria, it is recommended seminal plasma
proteins be further investigated to dene the relation-
ship with male and female fertility. Semen sampling at
12, 18 and 24 months of age should enable
the assessment of how early after puberty bulls
can be sampled to determine their adult concentration
of specic fertility-associated seminal plasma pro-
teins factors.
5. Metabolic and adaptive factors. IGF-1 has been
shown to be an important regulator of energy
metabolism in cattle. IGF-1 measured in pre-pubertal
Bos taurus bulls was positively correlated with adult
scrotal circumference and sperm motility and genet-
ically correlated with the age at rst calving of female
progeny and calving rate. Further, because of the
links between IGF-1 and growth traits (Thomas
et al. 2002), its relationship to fertility can be readily
investigated. Therefore, it is recommended that this
relationship and others be further investigated in
bulls. As reported earlier, reduced expression or
activity of the specic adaptive trait 11b-hydroxys-
teroid dehydrogenase in rodent testis Leydig cells
(measured in plasma) allows physiological concen-
trations of glucocorticoids to inhibit testosterone
biosynthesis, resulting in a disturbance in spermato-
genesis. Variation in the expression of this enzyme in
the testes of tropically adapted bulls may explain
some of the observed variation in per cent morpho-
logically normal sperm between bulls, related to
dierences in susceptibility to episodes of testicular
insults. The usefulness of measuring the activity of
this enzyme in seminal plasma could be assessed
using a semen and blood sampling schedule. As
leptin has been linked to both male and female
reproductive performance in numerous species, it is
recommended that the relationship between pre-
pubertal leptin concentrations and male and female
fertility be investigated.
6. Genes and genetic markers. The identication of
predictors of male andfemale fertility cansometimes be
labour intensive and expensive. Therefore, the identi-
cation of genes or genetic markers inuencing fertility
traits are appropriate candidates for improving male
and female fertility as they can reduce both the time and
expense of measurements and can improve genetic
response by aecting both the accuracy and the time of
selection (early-life predictors).
In conclusion, given the cost and eort in collecting the
phenotypes (physiological and endocrinological factors)
associated with reproduction, and the availability of
animal pedigrees, the logical strategy is to identify genetic
markers associated with QTL for a range of reproductive
traits. These genetic tests would enable identication of,
or selective production of, bulls with superior reproduc-
tive performance traits resulting in improved reproduc-
tive performance of their female progeny.
Conict of interest
None of the authors have any conict of interest to declare.
Author contributions
BM Burns, C Gazzola, RG Holroyd and MR McGowan all assisted
with the design of the review, literature search and editing of the paper.
BM Burns and C Gazzola were responsible for writing the rst drafts
of the paper. RG Holroyd, MR McGowan and J Crisp assisted with
later drafts of the paper.
References
Alves BCA, Unanian MM, Silva E, Oliveira
M, Moreira-Filho CA, 2005: Use of
RAPD markers for identifying Nelore
bulls with early reproductive maturation
onset. Anim Reprod Sci 85, 183191.
Anonymous 1986. Australian Bureau of
Statistics, 1986, Year Book of Australia.
Number 70. Aust. Bur. Stat., Catalogue
No. 1301.0.
Aravindakshan JP, Honaramooz A, Bart-
lewski PM, Beard AP, Pierson RA, Raw-
lings NC, 2000: Pattern of gonadotropin
secretion and ultrasonographic evaluation
of developmental changes in the testes of
early and late maturing bull calves. The-
riogenology 54, 339354.
Bagu ET, Cook SJ, Honaramooz A, Ara-
vindakshan JP, Huchkowsky S, Rawlings
NC, 2006: Changes in serum luteinizing
hormone (LH) concentrations in response
to luteinizing hormone releasing hormone
(LHRH) in bull calves that attained
puberty early or late. Theriogenology 66,
937944.
Bamualim WRB, Entwistle KW, Goddard
ME, 1984: Variation in fertility in Bos
indicus cross bulls. Anim Prod Aust 15,
263266.
Barendse W, Armitage SM, Kikpatrick BW,
Georges M, Moore SS, Womack JE,
Hetzel J, 1994: A genetic linkage map of
the bovine genome. Nat Genet 6, 227
238.
Barth AD, 2000: Bull Breeding Soundness
Evaluation manul, 2nd edn. The Western
Canadian Association of Bovine Practi-
tioners, pp. 175.
Bellin ME, Oyarzo JN, Hawkins HE, Zhang
H, Smith RG, Forrest DW, Sprott LR,
Ax RL, 1998: Fertility-associated antigen
on bull sperm indicates fertility potential.
J Anim Sci 76, 20322039.
Bishop MD, Kappes SM, Keele JW, Stone
RT, Sunden SLF, Hawkins GA, Solinas
Toldo S, Fries R, Grosz MD, Yoo J,
Beattie C, 1994: A genetic linkage map for
cattle. Genetics 136, 619639.
Boelhauve M, Sinowatz F, Wolf E, Paula-
Lopes FF, 2005: Maturation of bovine
oocytes in the presence of leptin improves
development and reduces apoptosis of in
vitro-produced blastocysts. Biol Reprod
73, 737744.
Brackett BG, Bosch P, McGraw RA, De-
Jarnette JM, Marshall CE, Massey JB,
Roudebush WE, 2004: Presence of plate-
let-activating factor (PAF) receptor in
bull sperm and positive correlation of
sperm PAF content with fertility. Reprod
Fertil Dev 16, 265.
Brandon C, Heusner G, Caudle A, Fayrer-
Hosken R, 1999: Two-dimensional poly-
acrylamide gel electrophoresis of equine
seminal plasma proteins and their corre-
lation with fertility. Theriogenology 52,
863873.
Brinks J, 1994: Relationships of scrotal
circumference to puberty and subsequent
reproductive performance in male and
female ospring. In: Fields M, Sand R
(eds), Factors Affecting Calf Crop. CRC
Press, Boca Raton, USA, pp. 363370.
Brinks J, McInerney MJ, Chenoweth PJ,
1978: Relationship of age at puberty in
heifers to reproductive traits in young
bulls. Proc West Sect Amer Soc Anim Sci,
29, 2830.
Cancel A, Chapman D, Killian G, 1997:
Osteopontin is the 55-kilodalton fertility-
associated protein in Holstein bull semi-
nal plasma. Biol Reprod 57, 12931301.
Casas E, Lundstra DD, Stone RT, 2004:
Quantitative trait loci for male reproduc-
tive traits in beef cattle. Anim Genet 35,
451453.
Chase C Jr, Kirby C, Hammond A, Olson T,
Lucy M, 1998: Patterns of ovarian growth
and development in cattle with a growth
hormone receptor deciency. J Anim Sci
76, 212219.
Coulter GH, Foote RH, 1979: Bovine
testicular measurements as indicators of
reproductive performance and their
relationship to productive traits in
cattle: a review. Theriogenology 11, 297
311.
Coulter GH, Rounsaville TR, Foote RH,
1976: Heritability of testicular size and
consistency in Holstein bulls. J Anim Sci
43, 912.
Crawford AM, Montgomery GW, Pierson
CR, Brown T, Dodds KG, Sunden SLF,
Henry HM, Ede AJ, Swarbrick PA,
Berryman T, Penty JM, Hill DF, 1994:
Sheep linkage mapping: nineteen linkage
groups derived from the analysis of pater-
nal half-sib families. Genetics 137, 573
579.
Cruickshank J, Dentine MR, Berger PJ,
Kirkpatrick BW, 2004: Evidence for
quantitative trait loci aecting twinning
rate in North American Holstein cattle.
Anim Genet 35, 206212.
Cundi LV, Nu n ez-Dominguez R, Dicker-
son GE, Gregory KE, Koch RM, 1992:
Heterosis for lifetime production in Her-
eford, Angus, Shorthorn and crossbred
cows. J Anim Sci 70, 23972410.
Cunningham P, England M, Young L,
Zimmerman D, 1979: Selection for ovu-
lation rate in swine: correlated response to
litter size and weight. J Anim Sci 48, 509
516.
Darwash AO, Lamming GE, Woolliams JA,
1999: The potential for identifying herita-
ble endocrine parameters associated with
fertility in post-partum cows. Anim Sci
68, 333347.
Eler J, Silva JA, Evans J, Ferraz J, Dias F,
Golden B, 2004: Additive genetic rela-
tionships between heifer pregnancy and
scrotal circumference in Nellore cattle.
J Anim Sci 82, 25192527.
Evans J, Golden B, Bourdon R, Long K,
1999: Additive genetic relationships be-
tween heifer pregnancy and scrotal cir-
cumference in Hereford cattle. J Anim Sci
77, 26212628.
Fischer K, Van Leyen K, Lovercamp K,
Manandhar G, Sutovsky M, Feng D,
Safranski T, Sutovsky P, 2005: 15-Lipox-
ygenase is a component of the mamma-
lian sperm cytoplasmic droplet.
Reproduction 130, 213222.
Fitzpatrick LA, Fordyce G, McGowan MR,
Bertram JD, Doogan VJ, De Faveri J,
Miller RG, Holroyd RG, 2002: Bull
selection and use in northern Australia:
2. Semen traits. Anim Reprod Sci 71, 39
49.
Foresta C, Flohe L, Garolla A, Roveri A,
Ursini F, Maiorino M, 2002: Male
fertility is linked to the selenoprotein
phospholipid hydroperoxide glutathione
peroxidase. Biol Reprod 67, 967971.
Fouchecourt S, Charpigny G, Reinaud P,
Dumont P, Dacheux J-L, 2002: Mamma-
lian lipocalin-type prostaglandin D2 syn-
thase in the uids of male genital tract:
putative biochemical and physiological
functions. Biol Reprod 66, 458467.
Fries R, Beckmann JS, Georges M, Soller
M, Womack JE, 1989: The bovine gene
map. Anim Genet 20, 329.
Gatti J-L, Castella S, Dacheux F, Ecroyd H,
Metayer S, Thimon V, Dacheux J-L, 2004:
Post-testicular sperm environment and
fertility. AnimReprod Sci 8283, 321339.
Georges M, Lathrop M, Bouquet Y, Hilbert
P, Marcotte A, Schwers A, Roupain J,
Vassart G, Hanset R, 1990: Linkage
relationships among 20 genetic markers
in cattle. Evidence for linkage between
two pairs of blood group systems: B-Z
and S-F V respectively. Anim Genet 21,
95105.
Gerena R, Irikura D, Urade Y, Eguchi N,
Chapman D, Killian G, 1998: Identica-
tion of a fertility-associated protein in bull
seminal plasma as lipocalin-type prosta-
glandin D synthase. Biol Reprod 58, 826
833.
Gonda MG, Arias JA, Shook GE, Kirkpa-
trick BW, 2004: Identication of an ovu-
lation rate QTL in cattle on BTA14 using
selective DNA pooling and interval map-
ping. Anim Genet 35, 298304.
Gong J, Bramley T, Webb R, 1991: The
eect of recombinant somatotropin on
ovarian function in heifers: follicular
population and peripheral hormones. Biol
Reprod 45, 941949.
Hahn J, Foote RH, Seidel GE Jr, 1969a:
Testicular growth and related sperm
output in dairy bulls. J Anim Sci 29,
4147.
Hahn J, Foote RH, Cranch ET, 1969b:
Tonometer for measuring testicular con-
sistency of bulls to predict semen quality.
J Anim Sci 29, 483489.
Haley CS, Lee GJ, Fordyce M, Baxter G,
Land RB, Webb R, 1989: Study of LH
response to GnRH in the young male as a
criterion of genetic merit for female
reproduction in sheep. J Reprod Fertil
86, 119133.
Harper M, 1989: Platelet activating factor: a
paracrine factor in preimplantation stages
of reproduction. Biol Reprod 40, 907
913.
Holroyd RG, Doogan VJ, De Faveri J,
Fordyce G, McGowan MR, Bertram JD,
Vankan DM, Fitzpatrick LA, Jayawardh-
ana GA, Miller RG, 2002: Bull selection
and use in northern Australia: 4. Calf
output and predictors of fertility of bulls
in multiple-sire herds. Anim Reprod Sci
71, 6779.
Jacobs K, Mattheeuws M, Van Poucke M,
Van Zeveren A, Peelman LJ, 2002: Char-
acterization of the porcine FABGL gene.
Anim Genet 33, 220223.
Kaneko H, Noguchi J, Kikuchi K, Akagi S,
Shimada A, Taya K, Watanabe G, Ha-
segawa Y, 2001: Production and endo-
crine role of inhibin during the early
development of bull calves. Biol Reprod
65, 209215.
Kaneko H, Noguchi J, Kikuchi K, Hasega-
wa Y, 2003: Molecular weight forms of
inhibin A and inhibin B in bovine testes
change with age. Biol Reprod 68, 1918
1925.
Kappes SM, Bennett GL, Keele JW, Ech-
ternkamp SE, Gregory KE, Thallman
RM, 2000: Initial results of genomic scans
for ovulation rate in a cattle population
selected for increased twinning rate. J
Anim Sci 78, 30533059.
Killian G, Chapman D, Rogowski L, 1993:
Fertility-associated proteins in Holstein
bull seminal plasma. Biol Reprod 49,
12021207.
King RG, Kress DD, Anderson DC, Door-
bos DE, Burfening PJ, 1983: Genetic
parameters in Herefords for puberty in
heifers and scrotal circumference in bulls.
Proc West Sect Amer Soc Anim Sci 34,
1113.
Kmiec M, Kulig H, Wierzbicki H, 2006:
Polymorphism of the leptin gene and its
association with some reproductive per-
formance traits of boars. Tiera rztliche
Umschau 61, 7778.
Kohsaka T, Hamano K, Sasada H, Wanat-
abe S, Ogine T, Suzuki E, Nishida S,
Takahara H, Sato E, 2003: Seminal
immunoreactive relaxin in domestic ani-
mals and its relationship to sperm motility
as a possible index for predicting the
fertilizing ability of sires. Int J Androl 26,
115120.
Koots KR, Gibson JP, Smith C, Wilton JW,
1994: Analyses of published genetic
parameter estimates for beef production
traits. Anim Breed Abstr 62, 309335.
Land RB, 1973: The expression of female
sex-limited characters in the male. Nature
241, 208.
Lejeune H, Chuzel F, Sanchez P, Durand P,
Mather J, Saez J, 1997: Stimulating eect
of both human recombinant inhibin A
and activin A on immature Leydig cell
functions in vitro. Endocrinology 139,
47834791.
Lien S, Karlsen A, Klemetsdal G, Vage DI,
Olsaker I, Klungland H, Aasland M,
Heringstad B, Ruane J, Gomez-Raya L,
2000: A primary screen of the bovine
genome for quantitative trait loci aecting
twinning rate. Mamm Genome 11, 877
882.
Lovercamp K, van Leyen K, Safranski T,
Fischer K, Manandhar G, Sutovsky M,
Herring W, Sutovsky P, 2004: Arachidi-
nate 15-lipoxegenase (15-LOX) in the
sperm cytoplasmic droplet is a potential
fertility marker in boars. Proc Soc
Study Reprod, 37th Annual Meeting
2004, 142.
MacDonald RD, Deaver DR, Schanbacher
BD, 1991: Prepubertal changes in plasma
FSH and inhibin in Holstein bull calves:
responses to castration and(or) estradiol.
J Anim Sci 69, 276282.
Mackinnon MJ, Hetzel DJS, Taylor JF,
1989: Genetic and environmental eects
on the fertility of beef cattle in a tropical
environment. Aust J Agric Res 40, 1085
1097.
Mackinnon MJ, Taylor JF, Hetzel DJS,
1990a: Genetic variation and covariation
in beef cow and bull fertility. J Anim Sci
68, 12081214.
Mackinnon MJ, Hetzel DJS, Corbet NJ,
Bryan RP, Dixon R, 1990b: Correlated
responses to selection for cow fertility in a
tropical beef herd. Anim Prod 50, 417
424.
Mackinnon MJ, Corbet J, Meyer K, Burrow
HM, Bryan RP, Hetzel DJS, 1991:
Genetic parameters for testosterone re-
sponse to GnRH stimulation and scrotal
circumference in tropical beef bulls. Lvstk
Prod Sci 29, 297309.
Martinez-Velazquez G, Gregory KE, Ben-
nett GL, Van Vleck LD, 2003: Genetic
relationships between scrotal circumfer-
ence and female reproductive traits. J
Anim Sci 81, 395401.
Matsuzaki S, Uenoyama Y, Okuda K,
Wanatabe G, Kitamura N, Taya K,
Yamada J, 2000: Age-related changes in
the serum levels of inhibin, FSH, LH and
testosterone in Holstein bulls. J Reprod
Dev 46, 245248.
Matwee C, Kamaruddin M, Betts DH,
Basrur PK, King WA, 2001: The eects
of antibodies to heat shock protein 70 in
fertilization and embryo development.
Mol Hum Reprod 7, 829837.
McCosker TH, Turner AF, McCool CJ,
Post TB, Bell K, 1989: Brahman bull
fertility in a north Australian rangeland
herd. Theriogenology 27, 285300.
Meyer K, Johnston DJ, 2001: Estimates of
genetic parameters from random regres-
sion analyses of scrotal circumference
and days to calving in Brahmans. Proc
Assoc Advmt Anim Breed Genet 14,
357360.
Meyer K, Hammond K, Parnell PF, Mack-
innon MJ, Sivarajasingam S, 1990: Esti-
mates of heritability and repeatability for
reproductive traits in Australian beef
cattle. Lvstk Prod Sci 25, 1530.
Meyer K, Hammond K, Mackinnon MJ,
Parnell PF, 1991: Estimates of covari-
ances between reproduction and growth
in Australian beef cattle. J Anim Sci 69,
35333543.
Michael A, Thurston L, Rae M, 2003:
Glucocorticoid metabolism and reproduc-
tion: a tale of two enzymes. Reproduction
126, 425441.
Miyamoto A, Umezu M, Ishii S, Ishi S,
Furusawa T, Masaki J, Hasegawa Y,
Ohta M, 1989: Serum inhibin, FSH, LH
and testosterone levels and testicular
inhibin content in beef bulls from birth
to puberty. Anim Reprod Sci 20, 165178.
Morris CA, Cullen NG, 1994: A note on
genetic correlations between pubertal
traits of males or females and lifetime
pregnancy rate in beef cattle. Lvstk Prod
Sci 39, 291297.
Morris CA, Baker RL, Cullen NG, 1992:
Genetic correlations between pubertal
traits in bulls and heifers. Lvstk Prod Sci
31, 221234.
Morris CA, Bennett GL, Johnson D, 1993:
Selecting on pubertal traits to increase
beef cow production. Proc NZ Soc Anim
Prod 53, 427432.
Morris CA, Verkerk GA, Wilson JA, 1999:
Angus selection herd reproductive data: a
genetic model for dairy cattle. Proc NZ
Soc Anim Prod 59, 169172.
Moschos S, Chan J, Mantzoros C, 2002:
Leptin and reproduction: a review. Fertil
Steril 77, 433444.
Moura AA, Erickson BH, 1997: Age-related
changes in peripheral hormone concen-
trations and their relationships with testes
size and number of Sertoli and germ cells
in yearling beef bulls. J Reprod Fertil 111,
183190.
Moura A, Koc H, Chapman D, Killian G,
2006: Identication of proteins in the
accessory sex gland uid associated with
fertility indexes of dairy bulls: a proteomic
approach. J Androl 27, 201211.
Mwansa P, Kemp R, Crews D Jr, Kastelic J,
Bailey D, Coulter G, 2000: Selection for
cow lifetime pregnancy rate using bull and
heifer growth and reproductive traits in
composite cattle. Can J Anim Sci 80, 507
510.
Nonneman DJ, Rohrer GA, 2003: Compar-
ative mapping of a region on chromosome
10 containing QTL for reproduction in
swine. Anim Genet 34, 4246.
ONeill CJ, ReidDJ, KellyMJ, Hill RA, 2000:
Variation in calving success in a Brahman
herd in northern Australia. Proceedings,
9th Congress of the Asian-Australasian
Association of Animal Production Socie-
ties and 23rd Biennial Conference of the
Australian Society of Animal Production:
Animal Production for a Consuming
World Vol. B, University of New South
Wales, Sydney, Australia, p.150.
Parent S, Leevre L, Brindle Y, Sullivan R,
1999: Bull subfertility is associated with
low levels of a sperm membrane antigen.
Mol Reprod Dev 52, 5765.
Perry VEA, Chenoweth PJ, Post TB, Munro
RK, 1990a: Fertility indices for beef bulls.
Aust Vet J 67, 1316.
Perry VEA, Munro RK, Chenoweth PJ,
Bodero DAV, Post TB, 1990b: Relation-
ships among bovine male and female
reproductive traits. Aust Vet J 67, 45.
Post TB, Christensen HR, Seifert GW, 1987:
Reproductive performance and produc-
tive traits of beef bulls selected for dier-
ent levels of testosterone response to
GnRH. Theriogenology 27, 317328.
Purvis IW, Piper LR, Edey TN, Kilgour RJ,
1988: The genetic relationship between
ovulation rate and testicular diameter in a
random-breeding Merino ock. Lvstk
Prod Sci 18, 3554.
Rohrer GA, Alexander LJ, Keele JW, Smith
TP, Beattie CW, 1994: A microsatellite
linkage map of the porcine genome.
Genetics 136, 231245.
Roncoletta M, Morani Eda S, Esper CR,
Barnabe VH, Franceschini PH, 2006:
Fertility-associated proteins in Nelore
bull sperm membranes. Anim Reprod
Sci 91, 7787.
Roncolleta M, Kata SR, Womack JE,
Amaral MEJ, 2002: Genome mapping of
the bovine seminal plasma A3 gene
(BSPA3). Anim Genet 33, 397398.
Roudebush W, Diehl J, 2001: Platelet-acti-
vating factor content in boar sperm cor-
relates with fertility. Theriogenology 55,
16331638.
Roudebush WE, Massey JB, Elsner CW,
Shapiro DB, Mitchell-Leef D, Kort HI,
2005: The signicance of platelet-activat-
ing factor and fertility in the male pri-
mate: a review. J Med Primatol 34, 2024.
Royal MD, Darwash AO, Flint APF, Webb
R, Lamming GE, Wooliams JA, 2000:
Estimation of genetic variation in the LH
response to a GnRH challenge in
pre-pubertal Holstein-Friesian heifers.
Proc Brit Soc Anim Sci, Winter Meeting.
British Society of Animal Science, Peni-
cuik, UK, pp. 15.
Sharpe R, McKinnell C, Kivlin C, Fisher J,
2003: Proliferation and functional matu-
ration of Sertoli cells, and their relevance
to disorders of testis function in adult-
hood. Reproduction 125, 769784.
Smith C, Simpson SP, 1986: The use of
genetic polymorphisms in livestock
improvement. J Anim Breed Genet 103,
205217.
Smith BA, Brinks JS, Richardson GV,
1989a: Estimation of genetic parameters
among breeding soundness examination
components and growth traits in yearling
bulls. J Anim Sci 67, 28922896.
Smith BA, Brinks JS, Richardson GV,
1989b: Relationships of sire scrotal cir-
cumference to ospring reproduction and
growth. J Anim Sci 67, 28812885.
Soller M, Beckman JS, 1982: Restriction
fragment length polymorphisms and
genetic improvement. Second World Con-
gress on Genetics Applied to Livestock
Production, Madrid, Spain 6, 396404.
Spinaci M, Volpe S, Bernardini C, De
Ambrogi M, Tamanini C, Seren E, Gale-
ati G, 2005: Immunolocalization of heat
shock protein 70 (Hsp70) in boar sper-
matozoa and its role during fertilization.
Mol Reprod Dev 72, 534541.
Splan RK, Cundi LV, van Vleck LD,
1998: Genetic parameters for sex-specic
traits in beef cattle. J Anim Sci 76,
22722278.
Sprott LR, Harris MD, Forrest DW, Young
J, Zhang HM, Oyarzo JN, Bellin ME, Ax
RL, 2000: Articial insemination in beef
females using bovine sperm with a detect-
able fertility-associated antigen. J Anim
Sci 78, 795798.
Steger K, Failing K, Klonisch T, Behre HM,
Manning M, Weidner W, Hertle L, Berg-
mann M, Kliesch S, 2001: Round sper-
matids from infertile men exhibit
decreased protamine-1 and -2 mRNA.
Hum Reprod 16, 709716.
Stewart BL, Roser JF, 1998: Eects of age,
season, and fertility status on plasma and
intratesticular immunoreactive (ir) inhibin
concentrations in stallions. Dom Anim
Endocrinol 15, 129139.
Sutovsky P, 2003: Ubiquitin-dependent pro-
teolysis in mammalian spermatogenesis,
fertilization, and sperm quality control:
killing three birds with one stone. Micro
Res Tech 61, 88102.
Thomas MG, Enns RM, Hallford DM,
Keisler DH, Obeidat BS, Morrison CD,
Hernandez JA, Bryant WD, Flores R,
Lopez R, Narro L, 2002: Relationships
of metabolic hormones and serum glu-
cose to growth and reproductive devel-
opment in performance-tested Angus,
Brangus and Brahman bulls. J Anim
Sci 80, 757767.
Toelle VD, Robison OW, 1985: Estimates of
genetic correlations between testicular
measurements and female reproductive
traits in cattle. J Anim Sci 60, 89100.
Vargas CA, Elzo MA, Chase CC Jr, Cheno-
weth PJ, Olson TA, 1998: Estimation of
genetic parameters for scrotal circumfer-
ence, age at puberty in heifers, and hip
height in Brahman cattle. J Anim Sci 76,
25362541.
Walkley JRW, Smith C, 1980: The use of
physiological traits in genetic selection for
litter size in sheep. J Reprod Fertil 59, 83
88.
Wheaton J, Godfrey R, 2003: Plasma LH,
FSH, testosterone, and age of puberty in
ram lambs actively immunized against an
inhibin alpha-subunit peptide. Therioge-
nology 60, 933941.
Wimmers K, Lin CL, Tholen E, Jennen
DGJ, Schellander K, Ponsuksili S, 2005:
Polymorphisms in candidate genes as
markers for sperm quality and boar fer-
tility. Anim Genet 36, 152155.
Yilmaz A, Davis ME, Simmen RCM, 2004:
Estimation of (co)variance components
for reproductive traits in Angus beef
cattle divergently selected for blood serum
IGF-I concentration. J Anim Sci 82,
22852292.
Yong-Jun Y, Yu-Jing C, Shu-Min B, Sha P,
Wei-Min L, En-Kui D, 2006: Leptin-
directed embryo implantation: leptin reg-
ulates adhesion and outgrowth of mouse
blastocysts and receptivity of endometrial
epithelial cells. Anim Reprod Sci 92, 155
167.
Submitted: 24 Aug 2010; Accepted: 16 Dec
2010
Authors address (for correspondence): BM
Burns, The University of Queensland, Centre
for Animal Science, Queensland Alliance for
Agriculture and Food Innovation, PO Box
6014, Red Hill, Rockhampton, Queensland
4701, Australia. E-mail: brian.burns@deedi.
qld.gov.au or b.burns@uq.edu.au

Burns Et Al. 2011. Male Reproductive Traits and Their Relationship To Reproductive Traits in Their

Încărcat de

Informații document

Descriere originală:

Titlu original

Drepturi de autor

Formate disponibile

Partajați acest document

Partajați sau inserați document

Opțiuni de partajare

Vi se pare util acest document?

Este necorespunzător acest conținut?

Drepturi de autor:

Formate disponibile

Burns Et Al. 2011. Male Reproductive Traits and Their Relationship To Reproductive Traits in Their

Încărcat de

Drepturi de autor:

Formate disponibile

Review Article

Male Reproductive Traits and Their Relationship to Reproductive Traits in Their

S-ar putea să vă placă și