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

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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

To cite this version:

Original

article

Selection

on

testis size

as an

indicator

of

_maturity

in

_growing

animals.

II

Correlated

_responses

in

_reproductive

rate

WG

Hill

PJ Marks

2

JC Jenkins

1

RB Land

2

1 Institute of Animal Genetics,

University

of Edinburgh,

2

West Mains _{Road, Edinburgh} EH9 _3JN;

2

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;

_E

_pertence

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 *

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

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

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

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

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:

_C

_L

_w/CLT

=

(r

AL

whw)/(rALThT)

where,

for

_example,

_C

_L

_{w, r}

_ALw

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

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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