Hill, WG

Jenkins, JC

Land, RB

Marks, PJ

English

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Original article
Selection on testis size as an indicator
of maturity in growing animals.
II Correlated responses
in reproductive rate
WG Hill PJ Marks2 JC Jenkins1 RB Land2
1 Institute of Animal Genetics, University of Edinburgh,
2 
West Mains Road, Edinburgh EH9 3JN;
AFRC Institute of Animal Physiology and Genetics Research,
Edinburgh Research Station, Roslin, Midloth%an EH25 9PS, UK*
(Received 2 October 1989; accepted 15 February 1990)
Summary - Selection was undertaken in replicated lines of mice for 11 generations high
and low on 5 wk body weight (HX, LX), on 5 wk testis weight (XH, XL), and on indices
in which body and testis weight were selected in the same (HH, LL), and in opposite
directions (HL, LH). There were correlated responses in number born in the 1st litter,
with differences between pairs of lines averaged over replicates and the last 5 generations
of: HX-LX = 2.2, XH-XL = 2.5, HH-LL = 1.0, HL-LH = -0.2, each with standard error
of 0.6. The control mean litter size was 10.3. Differences were only partly removed by
phenotypic correction for body weight, and limited data indicated that ovulation rate
responded little more than litter size. Previous experiments suggesting that litter size can
be changed by selecting on testis size are confirmed, but some of this response is associated
with body weight change.
reproduction / growth / testis / selection / mouse
Résumé - Sélection sur la taille des testicules considérée comme un indicateur de
la maturité des animaux en croissance. II Réponses corrélées sur les performances
de reproduction. Une e;Epertence de sélection chez la souris a été conduite pendant 11
générations, vers le haut (H) et vers le bas (L) selon plusieurs critères: masse corporelle
chez le mâle à 5 semaines (lignées HX, LX); masse testiculaire à 5 semaines (XH, XL);
indices combinant ces deux caractères, dans le même sens (HH, LL) ou en sens opposés
(HL, LH). Chaque expérience a été répétée 2 fois. Des corrélations entre le nombre
d’animaux nés en première portée et les critères cités ci-dessus ont été observées. En
moyenne les différences entre lignées haute et basse ont été les suivantes, pour les cinq
dernières générntions: HX-LX = 2,2; XH-XL = 2,5; HH-LL = 1,0; HL-LH = -0,2; avec
un écart type de 0,6. La taille de portée moyenne dans les 4 lignées témoins était de
10,3. Les différences ne sont que partiellement supprimées par une correction phénotypique
tenant compte de la masse corporelle, et des données partielles indiquent que la réponse
est légèrement plus élevée sur le taux d’ovulation que sur la taille de portée. Les résultats
d’expériences antérieures suggérant que la taille des portées pouvait être modifiée par
* Formerly AFRC Animal Breeding Research Organisation
une sélection à partir de la taille des testicules sont confirmés, mais cette réponse est
partiellement associée à une modification de la masse corporelle.
reproduction / croissance / testicule / sélection / souris
INTRODUCTION
It has been suggested that, because the same hormones are involved in gonadal
development and pituitary response in both males and females, testis size of the
male is an indicator of ovulation rate and thus litter size of his female relatives
(Land, 1973). In a previous experiment with mice (Islam et al, 1976), selection on
testis weight at 11 wks gave a correlated response in ovulation rate but not in litter
size. Similarly, correlated response in testis size was obtained from selection for
ovulation rate in pigs, but this was not associated with any substantial change in
litter size (Cunningham et al, 1979; Johnson and Neal, 1988). Selection in sheep for
juvenile testis size, corrected for body weight, led to little or no change in ovulation
rate but to more pronounced responses in mature body weight (Land et al, 1980;
Haley et al, 1989). Other workers have found some evidence of a correlation between
testis size and litter size or ovulation rate in sheep (Ricordeau et al, 1979, 1986;
Purvis et al, 1988), cattle (Toelle and Robison, 1985a) and pigs (Schinckel et al,
1983; Toelle and Robison, 1985b; see Haley et al (1989) for review). Selection for
litter size in mice led to correlated changes in testis weight, even after adjustment
for body weight (Eisen and Johnson, 1981).
The present experiment was designed to evaluate the efficacy of selection on
testis size as an indicator of degree of maturity, with the aim of changing the
relation between early growth rate and mature size. Selection was practised high
and low on body weight, on testis weight, and on indices in which selection was
practised in the same and opposite directions, all on mice of 5 wks of age. The
responses in testis size and body weight at different ages are reported elsewhere
(Hill et al, 1990). Because body size is itself correlated with both testis size and
ovulation rate, this experiment provides an opportunity to clarify the relationships
among the traits.
MATERIAL AND METHODS
The stocks used and basic design of the experiment are described in detail by Hill
et al (1990). In summary, there were 8 selected lines and 2 unselected control lines,
each replicated twice, maintained in 4 contemporary groups each of 4 selected lines
(either all single trait or all index) and 1 control. Selection was practised for high
or low body weight alone or males at 5 wks of age (lines designated HX, LX,
respectively), for high or low testis weight alone of hemicastrated males at 5 wks of
age (XH, XL), or for indices with both these traits selected in the same (index 1-
HH, LL), or in the opposite directions (index 2-HL, LH) (Land et al, 1980; Lee and
Land, 1985, Haley et al, 1989; Lee and Haley, 1990). Males were selected within full
sib families and females were sampled at random within families, as were males of
the controls (designated CC). There were 8 full sib families per line. Selection was
undertaken on each generation, except 7, until generation 12, ie for 11 generations
in all.
Litter size in first parity was recorded every generation on each family and on
spare matings, usually a total of 12 in each line, and at generation 13 body weight
at mating was recorded and more matings were set up. (Generation number in this
paper refers to that of the offspring, ie litter size of generation 1 implies unselected
dams mated to selected sires.) At generation 8, an extra group of females were taken
for more detailed analysis, and at approximately 9 wks of age they were mated to
males of the same line and observed daily for vaginal plugs. At d 17 of gestation
(plug at d 0) these mice were sacrificed and the ovaries and uterus excised. Corpora
lutea as an estimate of ovulation rate and the number of live foetuses were counted,
and prenatal mortality calculated as their ratio (ie assuming all ova were fertilized).
Statistical analysis was undertaken as by Hill et al (1990). In essence the error
variance was computed from the variation between replicates of lines selected in the
same way. The error has only 8 degrees of freedom, but includes both drift variation
between replicates and variation between mice within replicates.
RESULTS
The litter size of each generation during the period of selection is shown in figures 1
and 2, averaged over replicates. Individual replicate means are given in table I for the
last few generations (9-12) as a simple summary of the responses, which includes
most information since responses accumulate. Table I also contains estimates of
litter size and body weight of the female at mating when recorded in generation 13.
Contrasts among pairs of lines, eg HX-LX between the high and low body weight
selected lines, are given in table II, which includes results pooled over generations 9-
13. As lines had approximately the same effective population size, most inbreeding
effects should be removed by comparing litter sizes of high and low lines.
There was a consistent divergent response in litter size associated with selection
on body weight alone (HX-LX = 2.2 born, averaged over generations 9-13, from
table II), on testis weight alone (XH-XL = 2.5) and, although less, also on index 1
(HH-LL = 1.0) where the 2 traits were selected in the same direction. The response
in litter size on the antagonistic indices (HL-LH = -0.2) was small. A difference of 2
mice is equivalent to about 20% of the mean, or 0.8 phenotypic standard deviations.
Fitting a phenotypic regression on weight at mating reduced, but did not eliminate,
the high-low contrasts, regardless of whether the lines had been selected on body
weight or testis weight (table II).
Results of the more detailed study of components of litter size conducted earlier
at generation 8 are given in table III, with contrasts summarised in table II. The
differences in litter size (ie number of live embryos) were largest in the testis
weight single (XH-XL) and index lines (HH-LL), and reduced but not eliminated
by correction for body weight. The body weight (HX-LX) lines differed little in
litter size or in body weight, the latter a quirk of this generation as responses were
generally obtained (Hill et al, 1990). Ovulation rate differences were similar to or
greater than those for litter size, and not completely removed by regression; but the
HL-LH difference was positive for ovulation rate and negative for litter size. There
was no obvious pattern in prenatal survival (table III).
Insofar as any trend was detectable in numbers of failed matings, these generally
occurred in lines selected for low testis weight (table I).
DISCUSSION
It has been widely established that selection for body size in mice gives correlated
responses in litter size ( eg Falconer, 1973; Eisen, 1978) and similar results have been
obtained in lines selected in this laboratory from the same base population (Brien
et al, 1984). Evidence in other species is more equivocal: for example the genetic
correlation between body size and litter size in pigs appears to be small (Legault,
1971; Morris, 1975), but there are few estimates. In our previous experiment in
which selection was practised for testis weight at 11 wks, a positive correlated
response in ovulation rate and body weight was obtained, but litter size increased in
1 replicate and reduced in the other, with negligible mean change (Islam et al, 1976).
No explanation other than sampling for this inconsistency between experiments,
indeed between replicates, has been identified. Selection for ovulation rate in pigs
has changed ovulation rate substantially, but not litter size (Cunningham et al,
1979; Johnson and Neal, 1988).
In the present experiment, positive correlated responses have occurred in litter
size from selection on both 5 wk body weight alone and on 5 wk testis weight alone,
leading to a divergence of some 20% of the mean in each case. Body weight and
testis weight are, however, positively correlated, both phenotypically and, judging
by most of our results (Hill et al, 1990), genetically. Our data on ovulation rate
are much more scanty, but the indications are that it did not respond substantially
more than did litter size because changes in embryonic survival were small. The
HH, LL index lines showed less correlated response in litter size than the single
trait lines, the HL, LH index lines almost none. The data from Hill et al and table
II are summarized in table IV.
It is not easy to combine these results into a coherent whole. The relative
correlated response in litter size (L) to selection on body weight (W) or testis
weight (T) is, with equal selection intensities: CLw/CLT = (ALwhw)/(rALThT)
where, for example, CLw, rALw and h! denote the correlated response in litter
size to selection on body weight, the genetic correlation of these traits and the
heritability of body weight, respectively (Falconer, 1989). For the single trait
selection, taking hw = 0.26 and hT = 0.48 from within family selection (Hill et
al, 1990), rALW/!ALT = 1.2. The other indication that both traits were similarly
correlated is from the selection on index 2 (HL, LH), where little correlated response
was observed in litter size. The smaller correlated response in litter size to HH, LL
selection is surprising because the divergence between them in both body weight
and testis weight was similar to that in the single trait lines, but this could just be
a sampling error (table II).
The overall conclusion from this experiment, which agrees with findings of Eisen
and Johnson (1981), is that both body weight and testis weight influence litter
size independently. In the accompanying paper (Hill et al, 1990) it was shown that
selection for increased testis size in immature animals led to a small reduction
in mature weight. This result, coupled with the increased litter size, suggests that .
selection for testis size can lead to increased female reproductive efficiency, as found
by Lee and Haley (1990) with sheep, but that it should be regarded as a supplement
to, rather than replacement for, direct selection on litter size.
ACKNOWLEDGMENTS
This work was supported by a grant from the Agricultural and Food Research
Council. We are very grateful to Roberta Wallace, Ann Walker and staff of the
mouse house for technical assistance, and to Gene Eisen, Douglas Falconer and Chris
Haley for comments on a draft of this paper. Roger Land initiated the experiment
reported here and died after lab work had been completed. He is greatly missed.
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Selection on testis size as an indicator of maturity in growing animals. II Correlated responses in reproductive rate

WG Hill

PJ Marks

JC Jenkins

RB Land

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Jenkins JC

Marks PJ

Hill WG

Land RB

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Selection on testis size as an indicator  of maturity in growing animals II Correlated responses in reproductive rate

Effects of selection on growth, body composition and food intake in mice. I1. correlated responses in reproduction.

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Selection on testis size as an indicator of maturity in growing animals. II Correlated responses in reproductive rate

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