Genetic analyses of Bantam and selected low-weight White Plymouth Rock chickens and their crosses. II. Onset of sexual maturity and egg production

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Genetic analyses of Bantam and selected low-weight

White Plymouth Rock chickens and their crosses. II.

Onset of sexual maturity and egg production

Ea Dunnington, Pb Siegel

To cite this version:

Original

article

Genetic

_analyses

of Bantam

and selected

_low-weight

White

_Plymouth

Rock chickens

and their

crosses.

II.

Onset of

sexual

_maturity

and

_egg

_production

EA

_Dunnington

PB

_Siegel

Virginia Polytechnic

Institute and State

_University

Poultry

Science

_{Department, Blacksburg,}

VA

_2l!061-0332,

USA

(Received

30

_April

1990;

accepted

18

_January

₁₉₉₁₎

Summary - Two

_generations

of crosses between a

_population

of White

Plymouth

Rock Bantams and a line of White

_Plymouth

Rocks selected for low

_{body weight}

for 31

_generations

were

_{produced. Characteristically,}

the Bantams had

_produced

a

_high

proportion

of normal eggs, but

hen-day

normal egg

production

in this

population

was low. The hens selected for low

_body

_weight

also

_produced

a

_{high proportion}

of normal _eggs, but age at sexual

_maturity

had been

_{greatly delayed}

as a correlated _{response to} selection. In the 16

_{populations involving parental}

lines and crosses

_(Fi,

_F2and

_{backcrosses),}

_age at onset of sexual

_maturity

_{and egg}

_production

traits were measured.

_Comparisons

of these

populations suggested

that age at sexual

maturity

was influenced

_by

sex

_{linkage, by}

one or more genes with

major

effects and

_by

_{other genes with lesser} effects. When

_compared

to

performance

of the

parental populations,

some measures of

_reproductive

fitness were

improved by crossing

(age

at first semen

_production,

_age at first egg,

hen-day

normal egg

production).

Other traits were not

_{changed by crossing}

_(percent

normal eggs, duration of

fertility).

selection

_/

Bantam

_/

chickens

_/

sexual _maturity

_/

egg production

Résumé - _{Analyses génétiques} de deux _lignées de _{poules Plymouth} Rock _Blanche, l’une Bantam et l’autre sélectionnée pour un faible poids, et de leurs croisements. II. _Apparition de la maturité sexuelle et ponte. Deux

générations

de croisement ont été

_produites

à

_partir

d’une

_population

de

_{poules Plymouth}

Rock Blanche Bantam et d’une

lignée

de

_Plymouth

Rock Blanche sélectionnée _pour un

faible poids corporel pendant

31

générations.

D’une ma!,ière

_{caractéristique,}

les Bantam

produisaient

une

_proportion

élevée

d’oeufs

!cormaux, mais la

production journalière d’oeufs

normaux dans cette

_population

était

faible.

Les

_poules

sélectionnées _pour un

_{faible poids corporel produisaient}

aussi une

_proportion

élevée

_d’ceufs

_{normaux, mais}

_l’âge

à la maturité sexuelle était

_fortement

augmenté,

en

_réponse

indirecte à la sélection. Dans les 16

_{populations impliquant}

les

lignées parentales

et les croisements

_(F

_l

_,

_F

₂

et, croisements en

_retour),

_l’âge

à la maturité sexuelle et les caractères de _ponte étaient mesurés. Les

_comparaisons

entre ces

_populations

suggèrent

que

l’âge

à la maturité sexuelle est

in

f

i

uencé par

des

_gènes

liés au _{sexe, par} un ou

*

plusieurs gènes

à

_{effet majeur}

_{et par} d’autres

_gènes

à

_effets

moins

_importants.

Relativement aux

_{populations parentales,}

certaines mesures de

l’aptitude reproductive

étaient améliorées par le croisement

(âge

à la

première production

de semence,

âge

au

_premier

_oeuf,

_production

journalière d’ceufs

normaux).

Les autres caractères n’étaient pas

modifiés

par le croisement

(pourcentage

d’ceufs

normaux, durée de la

période

fertile).

sélection

_/

Bantam

_/

poule

/

maturité sexuelle

_/

ponte

INTRODUCTION

Artificial selection for traits of economic

_importance

in domestic animal

species

often results in reduced

_reproductive

fitness. This effect is

_particularly

common

when

_growth

rate and

_growth

patterns

are altered

(Siegel

and

Dunnington,

1985).

A finite and often limited

_pool

of resources available to an individual at _any

_given

time must be allocated to all

_needs,

_{including growth,}

_maintenance,

_deposition

of fat and

protein,

resistance to infectious

_agents,

and

_reproduction

_(Dunnington,

1990).

Intense selection for one or a few of these factors may leave the individual

without sufficient resources for the others

(Lerner,

_1954;

_Dunnington,

1990).

Long-term

selection for lower

_{body weight}

in White

Plymouth

Rock chickens has been

_{accompanied by many}

correlated _{responses, including} reduced

_appetite

and

_impaired

_{reproductive capabilities}

_(Dunnington

et

_{al, 1984; Dunnington}

and

Siegel,

1985).

Lack of

_appetite

in such a line

_developed

in our

_laboratory

has become so

_pronounced

that

_mortality

from starvation occurs

_during

the first week.

_Many

of the

_pullets

that survive are anorexic - that

_is,

_they

eat

_enough

food on an

ad libitum basis to

survive,

but not

_enough

to attain sexual

_maturity.

When

force-fed,

these

_pullets

commence _egg

_production

in a short time

(Zelenka

et

_al,

_1988).

The

_pullets

that do

_mature,

either

_{by force-feeding}

or with ad libitum

_feeding,

generally

produce

a

_high

_proportion

of normal eggs. Several studies have detailed

differences in

_pullets

that do and do not mature at

_particular

_ages

_and/or

_particular

body

sizes in this

_population

_(Zelenka

et

_al,

_1986a,

_b,

_1987).

The

_long-term

selection

_experiment

in which these chickens were

_developed

has

reached a limit for low 8-wk

_body

_weight

_(Dunnington

et

_al,

_1987).

When the

population

mean for

_{body weight}

of

_pullets

at 8 wk of _age

_(age

at

_selection)

reaches m 170 g, many of the smallest individuals never become

_sexually

_mature,

effectively arresting

selection for lower

_{body weight}

in the next

_generation

_(Siegel

and

_Dunnington,

_1987).

When selection is relaxed

_(because

the smallest individuals do not

_reproduce),

the

_problem

of anorexia is alleviated in the next

_generation.

This selection limit has been

_approached

3 times in the last 6

_generations,

but has not

been broken. In an

_attempt

to

_study

this situation

_further,

White

_Plymouth

Rock Bantams were obtained to cross with chickens from this

_low-weight

selected line.

Characteristically,

the Bantams matured at _{rather young ages and}

_produced

a

_high

proportion

of normal eggs, but

hen-day

normal egg

production

was low.

_Generally,

heterosis for age at sexual

_maturity

is found

_(Komiyama

et

_al,

_1984).

_Therefore,

offspring

produced

by

crossing

low-weight

and Bantam lines should retain their small size but

_might

_improve

in

_reproductive

_{capabilities.}

The influence of a

_major

_gene on _age at sexual

maturity

in

_pullets

was

_reported

more than half a

_century

_ago

(Hays,

_1924;

Warren,

_1928,

1934).

More recent work

each with small effects. The

_{experiment reported}

here allows

_testing

of the

_major

gene

theory

for _age at sexual

_maturity

in chickens.

The

_objective

of this

_study

was to evaluate

_genetic

_aspects

of age at sexual

maturity

and egg

production

traits in

_parental,

_F

_l

_,

_F

_Z

and backcross

_populations

produced

from

_{matings involving}

White

_Plymouth

Rock Bantam and White

Plymouth

Rock

_low-weight

selected chickens. The influence of a

_major

_{gene and}

of

_sex-linkage

on age at sexual

_maturity

of these

_populations

was examined.

MATERIALS AND METHODS

White

_Plymouth

Rock Bantams

_(supplied

_by

CJ

_{Wabeck, University}

of

_Maryland)

and a line of White

_Plymouth

Rocks that had been selected for 31

_generations

for low 8-wk

_{body weight}

_(Dunnington

and

_Siegel,

₁₉₈₅₎

were crossed. The 4

_resulting

populations:

BB, BL,

LB and LL

_(first

letter

_designates

sire line and second letter

dam

_line)

were hatched on

_September

_15,

1988. These chicks were

_wingbanded,

vaccinated for Marek’s disease and raised on litter in floor _pens with ad libitum feed and water. At 18 wk _{of age, 20}

_randomly

chosen males _per

_population

were

moved into individual cages in an

_{environmentally}

controlled room with continuous

light

to

_provide

semen for

_production

of the next

_generation.

Random

_samples

of 50

_pullets

_per

_population

were housed in the same

facility.

For

pullets,

_{age and}

body weight

at sexual

_maturity

_(production

of first

_egg),

_weight

of first egg and egg

production

were recorded.

_Egg

_production

data were used to calculate

_percent

normal _eggs

_[%

NE =

(Number

of normal

eggs

/

total eggs

produced) -

100]

and

hen-day

normal _egg

_production

_[%

HDNEP =

(Number

of normal

eggs

/ Number

of

_days

each hen was in

_{production) -}

_100].

Parental,

and all

_possible

_F

_i

_,

_F

₂

and backcross chicks were

_produced

from the

4

_populations.

Details of the

_mating

scheme have been

_presented

_(Dunnington

and

Siegel,

1991).

Designations

for the 16

_populations

in this

_generations

are 4

_letters,

the first 2

_indicating

the sire’s line and the second 2 the dam’s line. Semen from 20 males per

population

was

_pooled

to inseminate the

_appropriate

females.

Seventy-five - 80 females per

population

were used to

_produce

eggs.

For the

_offspring

_produced

_(hatched

2

_May,

₁₉₈₉₎

_{by crossing}

of

_{BB, BL,}

LB and LL

_{chickens, randomly}

chosen

samples

of 15 males per line were

_placed

in _cages and checked

_weekly

from 6 wk of age for semen

_{production. Age}

at

_production

of first semen was recorded as the _age of sexual

_maturity

for each male.

Randomly

chosen

_samples

of 20 females _per line were housed in individual cages at 18 wk of _age.

_Age

and

_{body weight}

at

_production

of _{first egg} were

recorded,

as well as

_weights

of the first and the _{10th normal eggs laid.}

_Age

at first egg was

considered _age at sexual

_maturity.

_Egg

_production

of each

_pullet

was recorded for

60 consecutive d after onset of sexual

_maturity.

_Egg

_production

data were used

to calculate

%

NE and

%

HDNEP. Pullets that reached 265 d of _{age without}

maturing sexually

were

dropped

from the

_study.

At 185 and

_again

at 188 d of age, 10 females per line were

artificially

inseminated with

_pooled

semen from at least 10 males of an unrelated White

_Leghorn

line. Duration of

_fertility

was then assessed

by breaking open every egg

on the

_day

it was laid and

_classifying

it as fertile or

infertile eggs, she was assumed to be infertile and the

_day

of her last fertile egg was

recorded to

_designate

duration of

_fertility.

Analysis

of variance and Duncan’s

_multiple

range tests were conducted to

ascertain differences between lines in

_generation

1

_{(4 populations),}

and the same

populations

were

_analyzed

in

_generation

2 to _compare results for 2

_generations.

In

_generation

_2,

_progeny from the 16

_mating

combinations were

compared by

analyses

of variance and contrasts were conducted to ascertain differences due to

the

_following

effects:

_{parental, reciprocal,}

heterosis and recombination. The

specific

contrasts are defined in the footnote of table II.

Weights

were transformed to common

_logarithms

and

_percentages

to arc sine _square roots

_prior

to

_analyses.

Analysis

of the

_populations

in this

_study

allowed examination of the influence of a

_major

_gene on _age at sexual

_maturity.

Comparisons

of combined

_frequency

distributions of the backcrosses to one

_parental

line with combined

frequency

distributions of the

_parental

and

F

l

crosses indicate whether one locus or more

is involved

_{(Stewart, 1969).}

If there is no difference between these 2 sets of means, one locus is sufficient to

_explain

the situation.

RESULTS

Comparisons

of

_parental

and

_reciprocal

_F

_l

_populations

Results from the 4

_populations

in

_generation

1

_(BB,

_BL,

_LB,

and

_LL)

and the same

populations

in

_generation

2

_(BBBB,

_{BBLL, LLBB,}

and

_LLLL)

for age at sexual

maturity

in females were

_quite

similar

(table I). Age

at first egg was earliest in cross

BL,

latest in

_parental

line LL and intermediate for

_populations

BB and LB. This

difference in the

_reciprocal

F

l

populations suggested

a sire-line effect for the trait.

Both

_{body weight}

at first _{egg and}

_weight

of the first _egg were lowest in the _pure

Bantams,

and

_{progressively higher}

for lines

_BL,

LB and

LL, respectively.

Hens of the 4

_populations

_{produced essentially}

_{all normal eggs, but there} were differences in

%

HDNEP. This trait was lowest in

BB,

higher

in LL and

highest

in the

reciprocal

F

l

crosses

_{(table I).}

In addition to the

similarity

of mean _age at onset of egg

production

in the 2

_generations

of this

_study,

_frequency

distributions _{of age} at first

egg were also similar

(fig

1).

Comparisons

of 16

_populations

By

265 d of age all

pullets

in most lines had reached sexual

_maturity.

Numbers of

pullets

that did not

_begin

to

_produce

_eggs

_by

this _age were: 1

(BLLL),

2

(LBLL),

1

_(LLBB),

2

_(LLBL)

and 3

_(LLLL).

These few immature

_pullets

were omitted from

the

_analysis.

There were

_significant

differences between

_parental

populations

for all

traits

_{(table II)}

_{except %}

NE and duration of

_fertility

_(data

not

_shown).

In each

case, means were

_higher

for line L than line B.

Reciprocal

effects were

_significant

for

maturity

of

_males,

age and

body weight

at first egg of females and

weights

of 1st and 10th eggs. Influence of heterosis was evident for age at sexual

maturity

in

both sexes

_(males,

-11%,

_females,

-16%),

_{body weight}

at _{first egg}

_(6%)

and

%

HDNEP

_(45%).

Effects of recombination were

_significant

_only

for _age at _{first egg}

For _age at first _egg, lack of

_significant

differences when

_comparing

combined

frequency

distribution of the

_parental

BBBB and

_reciprocal

F

i

crosses to the combined

_frequency

distribution of the backcrosses to B

_(calculated

_x

₂

=

_3.25,

dF =

3,

theoretical

X

2

=

7.81)

indicated that ₁ locus is sufficient _to

_explain

this

situation. That

_is,

there _appears to be a

_major

_gene

_influencing

_age at sexual

frequency

distribution of the

_parental

LLLL and

_F

₁

crosses

(calculated

x2

=

_42.34,

dF =

7,

theoretical

X

2

=

14.1)

indicates the absence of such _a

major

_gene in LLLL

pullets.

Because there was a difference between the

_reciprocal

_F

₁

crosses in _age at

first egg, with each

F

l

cross of

_pullets

_resembling

more

_closely

its sire

_line,

this gene appears to be sex-linked. Contrasts within each set of 4 backcross

_populations

to

evaluate contribution of sire line

_provided

additional

_support

that

_pullets

have

inherited the gene

for

_early

sexual

_maturity

from their sires

_(see

_means, table

_II).

The situation for sexual

_maturity

for males is less clear because each male receives

half of the

_genetic

influence for the trait from each

_parent.

Contrasts between the backcrosses to B and the backcrosses to _{L in age} at first

_production

of semen,

however,

were

_{significant (see}

_{means, table}

_II),

_suggesting

a

_dosage

effect in which

individuals which were

75%

B matured at _{younger ages than those} which were

75%

L.

DISCUSSION

Genetic _{control of age} at sexual

_maturity

Shapes

of the

_frequency

distributions of age at first egg in

generation

1

_prompted

us to

_{produce generation}

2 for further

_study.

The overdominance of

_F

_l

cross BL

suggested

that an effect of sire line for sexual

_maturity

in females

_{(ie, sex-linkage)}

was

_present.

_Also,

the bimodal

shape

of the distribution for LL females

_implied

that

a

_major

_{gene may} be

_influencing

the trait. The ideas that onset of _egg

_production

is sex-linked and _may be influenced

_by

one or a few _genes with

_major

effects were

reported

in the literature

_early

in this

century

( eg,

Hays,

1924; Warren, 1928,

1934),

but later research has treated the trait as a

quantitative

_one, influenced

by many

genes, each with a small influence

_(eg,

Komiyama

et

al,

1984).

To examine

_genetic

control of sexual

_maturity

in more

_detail,

it was _necessary to measure the trait for

both sexes in the 16

populations.

Results for age at _{first egg in}

_pullets

were

_essentially

the same in

_generation

2 as in

generation 1,

including degree

of overdominance and similar

_frequency

distributions in the

parental

and

_reciprocal

F

1

populations.

The

_consistency

of these results lent credence to the theories

espoused.

In

_comparison

of male and female _progeny

_{(generation 2)}

for

_age

at sexual

maturity,

it was evident that the female progeny resembled their sires in age at

maturity

to a

_greater

extent than male progeny resembled their dams. This would

be

_expected

in cases of

_sex-linkage,

as

_daughters

would receive a sex-linked _gene

from their

_sires,

but no

_{corresponding}

_{gene from their}

_dams,

while sons would

receive one allele from each

_parent.

This

_phenomenon

held for the

_reciprocal

_{F 1’s,}

the

_F

₂

_’s

and the backcross

_populations

in this

_experiment.

From a

_genetic

_perspective,

_{body weight}

at first _egg and

_weight

of the first _egg

behaved in a fashion similar to _age at first _{egg in pullets.} These traits are

_closely

Changes

in fitness

Both Bantam and

_low-weight

_{parental populations}

exhibited some

degree

of

re-duced fitness as correlated _responses to artificial selection. The

_low-weight

_pullets

experienced

delayed

sexual

_maturity

and both

types

of

_{parental pullets}

had reduced

%

HDNEP.

_Crossing

the 2

_parental

_populations

resulted in

_considerable

overdom-inance in both of these

_traits,

_restoring

the lost

_reproductive

fitness.

In

_contrast,

neither

_{parental population experienced}

reduced fitness in terms of

%

NE or in duration of

_fertility.

As a

_result,

there was no

_improvement

in the

_F

_l

1 crosses or in _any

_subsequent

crosses for these traits.

_Thus,

reduction in fitness due

to artificial selection does not

_necessarily

influence all measures of fitness to the

same

_degree.

CONCLUSION

The results of this

_study

_strongly

_suggest

that age at sexual

_maturity

in chickens has a

_genetic

_component that is sex-linked and that the _{trait may} be influenced

_by

large

effects of one or a few _{genes and}

_by

_{other genes with minor} effects.

REFERENCES

Dunnington

EA

₍₁₉₉₀₎

Selection and homeostasis. In: Proc

_4th

World

_Congr

Genet

A

P

pI

Livestock

_Prod,

_Edinburgh,

_{Scotland, July 23-27,}

_16,

5-12

Dunnington

EA,

Siegel

PB

₍₁₉₈₅₎

_Long-term

selection for 8-week

_{body weight}

in

chickens - direct and correlated responses. Theor

Appl

Genet

_71,

305-313

Dunnington

EA,

Siegel

PB

₍₁₉₉₁₎

Genetic

_analyses

of Bantam and selected

low-weight

White

_Plymouth

Rock chickens and their crosses. I.

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immunore-sponsiveness

and carcass characteristics. Genet Sel Evol 141-148

Dunnington EA, Siegel

PB,

Cherry

JA

₍₁₉₈₄₎

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sexual

_maturity

as a

correlated _response to selection for reduced

_56-day

_{body weight}

in White

_Plymouth

Rock

pullets.

Arch

_{Geflugelkd 48,}

111-113

Dunnington

EA,

Zelenka

DJ,

Siegel

PB

₍₁₉₈₇₎

Sexual

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in selected lines of chickens. Proc Br Poult Breeders’ Round

_{Table, Edinburgh, Scotland, Sept}

16-18

Hays

FA

₍₁₉₂₄₎

_Inbreeding

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reference to

winter _egg

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Nat

_{58, 43-59}

Komiyama T,

Nirasawa

_K,

Maito

_M,

Yamada

_Y,

Onishi N

₍₁₉₈₄₎

Selection for _age

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treatments and

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