Genetic interaction between sire and population of mates in Drosophila melanogaster

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Genetic interaction between sire and population of

mates in Drosophila melanogaster

Cm Wade, Jw James

To cite this version:

Original

article

Genetic interaction

between

sire

and

_population

of

mates

in

_{Drosophila melanogaster}

CM

Wade*

JW James

University of

New South

_{Wales, Department of}

Wool and Animal

_Science,

PO Box 1,

Kensington,

NSW

_2033,

Australia

(Received

8

_May

1992;

accepted

3

_January

₁₉₉₄₎

Summary - A model

_experiment

was set up to examine the level of

_{genotype-environment}

interaction

_existing

between a sire and the

_population

from which its mates were drawn.

The character considered was left

_{sternopleural}

bristle number in

_{Drosophila melanogaster.}

A total of 128

_males,

scored for the trait, were mated to females of the same and another

strain. The characteristic was then measured in both the pure and crossbred progeny

and the heritabilities for the trait in each _group were determined. The

_genetic

correlation

between _pure and crossbred

_performance

_(t

standard

_error)

estimated from covariances, 0.59

_(!

_0.17),

was found to be

_{significantly}

different from one,

indicating

the presence of

genetic

interaction. The

_heritability

of

_{purebred performance}

_(by

_regression

_analysis)

was

found to be 0.29 and the

_heritability

of crossbred

_performance

0.11. The

_{corresponding}

average values from sib

analysis

were 0.40 and

0.24, respectively.

A

_comparison

of responses

from different selection

_{methods, incorporating}

the estimated _parameters, found that selection on the basis of sire’s own

_performance

led to the

_{largest improvement}

in the

performance

of crossbred progeny. The

implications

of the results are discussed.

genotype-environment interaction

_/

_genetic correlation between _purebred and

cross-bred _performance

_/

_{sternopleural} bristles

_/

_{Drosophila melanogaster}

Résumé - Interaction génétique entre _géniteur et _population des partenaires chez

Drosophila melanogaster. Une

expérience

modèle a été menée _pour examiner

l’importance

de l’interaction entre le

_géniteur

et la

_population

dont ses _partenaires sont issus. Le

caractère utilisé est le nombre de soies

_{sternopleurales}

sur le côté

gauche

chez

Drosophila

melanogaster.

Cent

_{vingt-huit mâles,}

contrôlés _pour le

_caractère,

ont été

_accouplés

à des

_femelles

de la souche elle-même et d’une autre souche. Les héritabilités ont été estimées dans les 2 souches. La corrélation

génétique

entre les caractères en souche pure

et en _croisement, de _0,59 f 0,17, était

_{significativement différente}

de 1,

indiquant

la

présence

d’une interaction

_génétique.

Les héritabilités du nombre de soies chez les souches

*

pures et

hybrides

sont

0,29

et

0,11 respectivement

par

régression parent-descendant

et

les valeurs

correspondantes

estimées par

analyse

des

germains

sont

_0,40

et

_0,24.

Une

comparaison

des

réponses prédites

selon

_différentes

méthodes de

sélection,

sur la base des

paramètres estimés,

montre que la sélection sur la

performance

_propre du

géniteur

donne

l’amélioration la

plus grande

de la

_performance

dans la descendance croisée.

interaction _{génotype-milieu}

_/

corrélation _génétique entre _performance pure et croisée

_/

soie _{sternopleurale}

_/

_{Drosophila melanogaster}

INTRODUCTION

The value of

_{crossbreeding}

to increase the

_efficiency

of

_production

has been

recognised

in many animal

_species.

The

_improvement

of

production

in the crossbred

is due

_primarily

to the manifestation of

heterosis,

or

hybrid

_vigour,

which indicates the _presence of non-additive _gene effects.

Standal

₍₁₉₆₈₎

_suggests

that if heterosis is due to overdominance then selection

on the basis of

purebred performance

will not result in

_{corresponding}

_improvement

in the crossbred. Selection on the basis of crossbred

performance,

or

combining

ability,

is

_complex.

In

_practice

such a scheme will be difficult _{to use,}

_particularly

when

populations

are small. If the

degree

of

_genetic

interaction

_occurring

between a sire and the

_population

of females to which it is mated is

_quantified,

then the choice of the

_optimal

selection method is facilitated.

It is

_possible

to determine the extent of

_genetic

interaction

_present

_using

2

methods. The interaction _may be

_{statistically}

estimated from

_parameters

obtained within a

_single

_generation

(Brun, 1982),

as in this _case, or derived from estimates

of variances and covariances realised in the course of selection

(Brun, 1984).

Brun

₍₁₉₈₂₎

defined

_parameters

to

_{statistically}

estimate the

_degree

of

_genetic

interaction for the

_particular

situation of

_genotype

_by

mate interaction within a

single generation.

These

parameters

are the

genetic

correlation between pure and

crossbred

_performances

_(rgp

_c

₎

and the relative

_heritability

of

_purebred

_performance

(h

2

)

compared

with the

_heritability

of crossbred

_performance

_(h!).

The

_parameters

renect

the different means

_by

which the interaction may be

expressed:

in one _case, as a

_change

in the

_ranking

of

_sires,

or in

_another,

as a difference in variance between

the

_purebred

and crossbred _progeny.

Should a

_{large genetic}

interaction be

_discovered,

then selection on the basis of

crossbred

_performance

will result in

_greater

_genetic

_progress. Should the interaction be

absent,

or

insignificant,

then selection within the

purebred

_may be

regarded

as

the method of choice.

When the

_genetic

interaction is not

_significant,

most of the _gene effects

_expressed

in the

purebred

will also be

expressed

in the crossbred progeny. Selection that

considers

only

performance

in the

_purebred

is desirable since it relies

only

on

individual

_performance

rather than on a _{progeny test} which _may reduce selection

intensity

and increase

_generation

interval.

In this

_study,

progeny variances were

analysed

to estimate

_genetic

_parameters

including

the

_genetic

correlations between _pure and crossbred

_performance,

pure and crossbred

performance

for left

sternopleural

bristle number in

Drosophila

melanogaster.

The

_parameters

were obtained with the aim of

_elucidating

the

opti-mal method of selection for the

improvement

of crossbred progeny

performance.

MATERIALS AND METHODS

Two random

_breeding

strains of

_{Drosophila melanogaster}

were

_employed

as source and tester stocks. The source stock contributed the

experimental

sires and the dams for

_purebred

_progeny, and the tester stock

_provided

dams for _{crossbred progeny.}

The source stock used was the Hunter

_Valley

wild-type

strain and the tester stock a

white-eyed

mutant strain. Both stocks were maintained as

_separate

random

_mating

populations.

At intervals of less than 12 h

_newly

_emerged

flies were

_separated

into sexes

for each strain

_type.

Once

_separated,

these flies were transferred to fresh bottles

containing

a semolina-based

_fly

medium. Males of the source strain were chosen

at

random,

scored for

_{left-sternopleural}

bristle

number,

and

_placed

in

_separate

numbered vials with 4 females each of their own and the tester strain. After 4 d the

males were discarded and the females

_placed

in

_pairs

of similar strain into

_laying

vials labelled with the sire number and a label

distinguishing

that

_pair.

Prior to

the _emergence of _progeny, females were removed from the vials and discarded.

A total of 150 sires were measured in 3 _{groups, 1 group in} each of 3 successive months. It was

_planned

to score left

_{sternopleural}

bristle number in 10 _progeny, 5

of each _sex, for each _progeny vial. In all 128 sires were included in the

_analysis.

The sire

_components

of variance for the 4 _progeny

_classes,

2 for each strain and 2

for each sex, were calculated

_using

a hierarchical

_analysis

of variance for unbalanced

data. The model was

_adjusted

for the effects of group

(fixed),

sire

(random),

vial

(random)

and random error

according

to the model:

where:

Yij

kl

= individual bristle

score; p =

progeny mean for each sex and strain

type;

gi = effect of the ith group;

si! = effect of the

jth

sire within the ith group;

vz!k = effect of the kth vial within the

jth

sire and the ith

group;

e2!kt = random _{error term.}

By

analysing

the data

_separately

for sexes, the presence or absence of sex

dimorphism

(Frankham, 1968)

could be established.

Progeny

class

_regressions

were

_analysed.

Coefficients were obtained for crossbred on

purebred performance,

within and between _sexes, and also for _progeny bristle score on sire bristle score

_according

to the model:

where:

Y

ij

=

p, =

progeny mean for each strain and sex

_type;

gi = effect of group ;

b =

regression

gradient;

Xij =

independent variable,

which

may be sire bristle

number,

purebred

male

bristle

number,

or

purebred

female bristle

number;

x = _mean bristle number for the

progeny classes

compared;

e

ij = random _{error term.}

The

_regressions

were used to determine covariances between

_offspring

and

_parent

for each _progeny class and for

_purebred

and crossbred

_performance.

Variances and standard errors for the covariance estimates were calculated.

Estimation of the interaction between sire and

_population

of mates

Heritabilities

Narrow-sense heritabilities were determined

_{by regression}

_analysis

with the

heri-tability

for any progeny class

being regarded

as twice the _progeny on sire

_regression.

Half-sib

_analysis

was used to estimate the

_heritability

for left

_{sternopleural}

bristle

score from

_partitioned

_components

of

_variance,

such that:

for _{any progeny class. Standard} errors were calculated

_according

to the method of Falconer

_(1983).

Genetic correlation between pure and crossbred

performance

The

_pooled

_genetic

correlation was estimated from variances and covariances

pooled

over crossbreds

(V,)

and

_purebreds

(Vp),

and between _pure and crossbreds

(cofp

c

)

according

to the

equation:

where:

rgp

c is the

pooled genetic

correlation between pure and crossbred

performance;

Vp

=[<Tspm+!]/2;

Vc = [O’!cm + 0’!cf]/2;

i cov p c =

!C0llgpmcm

₊ CO’US p fcf + _C0lJgpfcm’!

_COf

_Sc

_fpmj/

₄

_;

0

O’!pf’

O’!pm’

O’!cf’ O’!cm

are estimated sire

components

of variance for

_purebred

females,

purebred

males,

crossbred females and crossbred

males, respectively;

and

C0llgpmcm! COVpfcf, S fcm, pSCOV COVScfpm are covariances between sire

_components

for

the same _progeny classes.

The variance for the correlation was calculated as the variance of a ratio

The

pooled

correlation enabled the

_expected

level of interaction between the 2

breed

_types

to be assessed without

_{special regard}

to sex.

Direct and correlated selection _responses for increased crossbred

performance

The ratios of the correlated response per

generation

to individual

selection,

and the

correlated response to selection on

purebred

_progeny

performance

_against

direct

selection on the

_performance

of crossbred progeny were calculated.

CR;

= correlated

response in crossbred progeny from selection on

_sire;

CRp

= correlated

response in crossbred progeny from selection of sires on

purebred

progeny

test;

- R

e

= direct

response from selection of sires on crossbred _progeny

_test;

n = number of

progeny tested per

sire;

i

l

= standardised selection differential for individual

selection;

i

2

= standardised selection differential for

progeny tested sires.

Comparisons

were made on the basis of

_selecting

50 sires from _groups of

_1000,

2 000, 4 000,

10 000 and 20 000 individuals tested. If sires were _progeny tested then fewer sires could be tested. Selection

_intensity

was reduced as the number of _progeny tested per sire increased.

RESULTS

Partitioning

of variance

_components

Sire

_components

for

_purebred

progeny were

_{approximately}

double those for

cross-bred progeny.

Group

and sire effects were

_significant

in all progeny classes. The vial

Heritability

of left

_{sternopleural}

bristle score

The

_heritability

for left

_{sternopleural}

bristle number in the crossbred was lower than

that for the same character in the

purebred

(table II).

This difference is due to lower sire

_components

of variance for crossbred _progeny of both sexes. The heritabilities calculated for crossbred _progeny are not

_strictly

narrow sense heritabilities since

differences exist in levels of dominance and _gene

_frequencies

between the

_purebred

and crossbred

_populations.

Genetic correlations between _pure and crossbred

_performance

The

_pooled

estimate for the

_genetic

correlation between _pure and crossbred

₍₁₎₁

standard

_error)

was 0.59

_{(!0.17) (table III).}

The estimate differed

_{significantly}

from

Estimated _response ratios

Estimations revealed that in most cases individual selection of the sire’s own

performance

gave a

_superior

_response in the _progeny to direct selection on crossbred

progeny

performance,

which was in turn

_superior

to selection on the basis of

purebred

progeny

performance

(table IV).

Differences in heritabilities for pure

and crossbred progeny contributed to this

_result,

as did the reduction in

possible

selection

_intensity

_{with progeny}

_testing,

_offsetting

the benefits of increased selection

accuracy.

DISCUSSION

Genetic interaction between sire and

_partner

_population

has been found to occur with

_greater

_frequency

in traits related to fitness and heterotic

traits,

which

_usually

have low

_{heritability,}

than in traits with additive _{gene action}

_{(Brun, 1985).}

This

_study

found the

_genetic

correlation between pure and crossbred

(!

standard

error)

to be

_significant

_{(0.59 t 0.17),}

_supporting

the

_hypothesis

of

_{non-additivity.}

Left

_{sternopleural}

bristle number

_usually

behaves in an additive manner and

ex-hibits little or no heterosis. It _was,

_{therefore, surprising}

to find that the

_heritability

for the trait in the

_purebred

was

_higher

than that in the crossbred. Such a difference

is often an indicator of non-additive _gene action.

Estimates of

_heritability

for bristle number in

_{Drosophila melanogaster}

are

_wide,

ranging

from 0.14

_(Sheridan

et

_al,

₁₉₆₈₎

to 0.46

_(Howe

and

James,

1973).

The estimate of

_heritability

from

_regression

_analysis

in the

_purebred

_(0.29)

_agrees well with the

_expected

_heritability

of

_0.2-0.3,

while that from sib

_analysis

was somewhat

higher

than

_expected

_(0.40).

The

_regression

_analysis

estimate for the crossbred

(0.11),

is

_clearly

lower than was to be

_expected

from

_previous

studies while the

sib-analysis

estimate

_(0.24)

was in the

_expected

_range.

No estimate for

genetic

interaction between sire and mates has been

_previously

reported

for

_{sternopleural}

bristle number in

_Drosophila

_using

the statistical

ranging

from less than zero to

_greater

than 1. The few values for

laboratory

in-sects are scattered

_widely

(-0.32,

0.85 in Brown and Bell

(1980)

for eggs laid in

Drosophila

melanogaster,

and 0.4 for

_{pupal weight}

in Tribolium casteneum

_(Wong

and

_Boylan,

_1970)).

The

_comparison

of responses from individual selection in

sires,

and selection on

the basis of

_purebred

_progeny, and crossbred _progeny

_performances

when

_testing

resources are

_limited,

revealed that under the observed conditions

_(rgp

_c

=

0.59,

h)

=

0.29,

h! =

0.11)

there was little benefit in the use of _progeny

_testing

as an

aid to selection for increased crossbred

_performance.

With limited

_{testing capacity,}

selection on individual sire

performance

was found to

_generate

_superior

response

to that from selection on the basis of crossbred progeny

performance,

which was

in turn

_superior

to selection on the

performance

of

purebred

_progeny. This was

primarily

due to the

_higher

selection

_{intensity possible}

_using

mass

selection,

and to

a reduced

dependence

on sire

_prolificacy.

The accuracy of progeny

testing

is increased with the number of progeny tested

per sire.

However,

when

testing capacity

is

limited, increasing

the number of progeny

tested per sire decreases the number of sires able to be

represented

in the test. If

the number of sires

required

is

_fixed,

then the selection

intensity

is decreased as the

number of _{progeny per} sire increases. The

_optimum

_response from direct selection

on crossbred _progeny

performance

occurs at the

_point

of balance between effects

on selection _accuracy and selection

_intensity.

As

_{testing capacity}

is

_increased,

the

response from direct selection on crossbred

performance

increases relative to the

response from individual selection due to increased selection accuracy.

Robertson

₍₁₉₅₇₎

showed that the

_optimum

response from progeny

testing

was

achieved when the number of progeny

(n)

tested was:

where k describes the ratio of males recorded to the number selected and

_{h! is}

the

heritability

of crossbred

_performance.

The

_comparison

of

purebred

and crossbred progeny

testing

to

_improve

crossbred

performance

revealed that for every

testing capacity

and

family size,

direct selection

on crossbred

_{performance yielded}

_superior

_responses in the crossbred to those

resulting

from selection on the basis of

_purebred

progeny

performance,

a direct

result of the

_genetic

interaction between _pure and crossbred

_performance.

The use of _progeny

_testing

to evaluate sires for

_{crossbreeding performance}

in

livestock is

_{disadvantaged by}

some

practical

considerations.

First,

it is _necessary for

the breeder to maintain both source and tester dam

_populations

in order to _progeny test the sires. One of the dam

populations

will

produce

stud stock

_(source),

and the other commercial stock

_(tester).

Different

_management

_practices

may be

required

for the 2

_types

of stock.

Second,

there is a loss of

_production

in

_purebred

_progeny

when sires are selected for

_{crossbreeding}

merit and a

_significant

_genetic

interaction

is

_present.

_Finally,

the selection

_{lag occurring}

as a result of _progeny

_testing

reduces

selection response,

particularly

in

_larger

_species.

The

_{genetic gains}

able to be made

through

direct

selection

on crossbred progeny

performance

are

_unlikely

to

_outweigh

Harris

₍₁₉₇₆₎

_suggests

that the

optimal

selection

_approach

is to select on an index

of sire and crossbred progeny

performance.

An alternative

_approach

_may be to select sires for _progeny

_testing

on the basis of their own

_performance

and then make a

further selection on the

performance

of their _progeny, or on an index of individual

and _progeny

_performance

_(Cochran,

_1951).

In this case _{crossbred progeny would be}

used in the _progeny test.

Although

a

_genetic

interaction between the sire and

_population

of mates was

observed,

it was

insufficiently large

to warrant direct selection for _{crossbred progeny}

performance.

This was demonstrated

_by

the

comparison

of responses between

individual selection and selection on the

_performance

of crossbred _progeny. The

findings

suggest

that for both

_genetic

and economic reasons, selection on the basis

of individual

_performance

is the best selection method of those

examined, assuming

that the correlation between _pure and crossbred

_performance

is a

_positive

one.

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