Directional selection on body weight and hybrid dysgenesis in Drosophila melanogaster

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Directional selection on body weight and hybrid

dysgenesis in Drosophila melanogaster

D Higuet

To cite this version:

Original

article

Directional selection

on

body

weight

and

_hybrid

_dysgenesis

in

_{Drosophila melanogaster}

D

_Higuet

Université P & M

_Curie,

Laboratoire de

_Génétique

des

_Populations,

Mécanismes Moléculaires de la

_Spéciation,

Tour l,2, !,e

étage,

4 place

Jussieu,

75251 Paris, France

(Received

9 October

1990; accepted

20 March

₁₉₉₁₎

Summary - The influence of

_transposable

elements in

_generating

variation for

_body

weight

of

_{Drosophila melanogaster}

was

_{investigated by comparing}

the _response to artificial

divergent

selection in

_dysgenic

and

_nondysgenic

crosses

_using

2

_independent

_systems of

hybrid dysgenesis (PM

and

_IR).

Two

replicates of initially dysgenic

or

_nondysgenic

crosses

between Furnace Creek

_(IP)

and Gruta

_(RM)

strains were selected for increased and

decreased

_{body weight during}

13

_generations.

A _greater

_divergence

in selection response

was observed for the

_dysgenic

lines than for the

_{nondysgenic lines,}

but this difference

disappeared

when selection was relaxed. The selected lines were

_analysed

at

_generation

13 with _respect to their

_{dysgenesis properties,}

as well as to the number and nature of their P and I elements. There was no correlation between the characteristics of the P and I

elements in the selected lines and the

_intensity

of _{response to} selection for

_{body weight.}

In both types of crosses,

hybrid dysgenesis

induced modification in

_{body weight variance,}

probably by

I and I’-induced mutations.

hybrid dysgenesis

/

PM and IR _systems

_/

_{body weight}

_/

_{Drosophila melanogaster} Résumé - Sélection directionnelle sur le _poids des adultes et _dysgénèse des _hybrides chez _{Drosophila rnelanogaster.}

_L’aptitude

des éléments

transposables

à

_générer

de la

variabilité _pour le caractère

_poids

des adultes chez

_{Drosophila melanogaster,}

et donnant

ainsi une

_{plus grande prise}

à la _sélection, a été étudiée en _comparant la

_réponse

à une

sélection bidirectiorarcelle suivant _que le croisement

_originel

était ou non

_dysgénique

vis-à-vis des

_systèmes

PM et IR de

_dysgénèse

des

_hybrides.

Deux

_répliques

de

_chaque

_type

de croisement

_(dysgénique

ou non

dysgénique)

ont été réalisées entre les souches Furnace Creek

_(IP)

et Gruta

_(RM),

puis une sélection bidirectionnelle a été

appliquée

_pour un

poids

élevé des adultes ou _pour un

_{poids faible.}

Une

_{plus grande divergence}

de

_réponse

à la sélection a été observée

lorsque

le croisement initial était

dysgénique

_{par rapport} au cas où .il était non

_dysgénique.

Mais cette

_{différence disparaît quand}

la _pression de sélection est relâchée.

_{En fin}

de sélection

_{(génération}

_13),

les

_lignées

sélectionnées ont été

analysées

pour le nombre et la nature de leurs éléments P et I. Aucune corrélation n’a été mise en évidence entre les

_{caractéristiques}

des éléments P et I

_présents

dans les

_lignées

la

dysgénèse

des

_hybrides

induit des

modifications

de la variance du

poids

des

_adultes,

probablement

dues à des mutations induites par les éléments

transposables.

dysgénèse des hybrides

/

systèmes PM et IR

_/

_poids des adultes

_/

_Drosophila

melanogaster

INTRODUCTION

The

_discovery

of

_transposable

elements in the

Drosophila

genome has breathed new life into

_{population genetics. Transposable}

elements _may

_modify

the

_organisation

of the genome

by

mediating

deletions, translocations, transpositions, duplications

and

_inversions,

and are thus a source of

genetic

innovation. Whilst the mechanisms involved in

_{transposition}

are

_beginning

to be

understood,

the effect of

_transposable

element

_mobility

on

_generating

variation for

_quantitative

traits remains unclear. Both Gvozdev et al

₍₁₉₈₁₎

and

_Mackay

_{(1984, 1985),}

_using

the

_mdg-1

mobile element and P elements

_{respectively,}

have shown that

_transposable

elements can contribute to selection response. This may occur either

through preferential

insertion

_(Gvozdev

et

_al,

_1981),

or as

_transposable

element-induced

_variability

which

permits

a

_greater

selection _response

(Mackay, 1984, 1985).

However,

the observation of

_greater

selection response from

dysgenic

than from

_nondysgenic

crosses has not been

_repeated

_(Morton

and

_{Hall, 1985;}

Torkamanzehi et

_{al, 1988;}

_Pignatelli

and

Mackay,

1989).

In

_parallel,

several

_experiments

were

_performed

to ascertain the effect of

transposable

elements on fitness

_(for

review see

_Mackay,

₁₉₈₉₎

or the

_ability

of the PM

_{hybrid dysgenesis}

_system

to

_generate

mutations on the X chromosome that would affect bristle traits

_(Lai

and

_Mackay,

_1990).

In this

_report,

observations on the _response to selection from

_dysgenic

and

nondysgenic

crosses

_(for

both P-M and I-R

_systems)

are extended to another

quantitative

trait

_{(body weight).}

After selection

_ceased,

the

_relationship

between the _response attained and the

_{transposition}

of P and I elements was

_{investigated.}

Two

_independent

systems

of

_{hybrid dysgenesis}

associated with P and I

trans-posable

elements

_(the

P-M and I-R

_systems,

_{respectively)}

have been described

in

_{Drosophila melanogaster}

_(see

_Engels,

_1988;

and

_Finnegan,

_1989,

for

_reviews).

Dysgenesis

is due to

_{incompatibility}

between chromosomal determinants

_{(I or}

P

elements)

and extrachromosomal

_state,

defined as

_reactivity

in the I-R

_system

and as

_{susceptibility}

in the P-M

_system.

When males of

_{Drosophila melanogaster}

carry-ing

autonomous P elements on their chromosomes

_{(P males)}

are crossed to females

lacking

P sequences

(M females),

or

_carrying

defective P elements

_{(M’ females),}

the

_{dysgenesis syndrome}

can be observed. This takes the form of

_{transposition}

in the germ line of the

dysgenic

hybrids and,

in both sexes, may lead to

_gonadal

atro-phy

(GD

sterility; Engels,

1983).

Also involved in the

_syndrome

are an increase in

the level of

_mutation,

_{male recombination and chromosomal breaks and} rearrange-ments. If males

_bearing

active I elements

_{(I factor)}

are crossed to females

_lacking

these elements

_{(R females),}

the I factors

_transpose

and the Fl females _may

be-come sterile due to the death of their _progeny at the

_embryonic

_stage

_(SF

_sterility;

MATERIALS AND METHODS Strains

’

The Furnace Creek strain

_(captured

in

_California,

USA in

₁₉₈₁₎

is a weak P strain

(27%

GD

_sterility

_{by diagnostic}

cross

A)

and an inducer strain with

regard

to the IR

_system.

The Gruta strain

_(captured

in

_Argentina

in

₁₉₅₀₎

is an MR

_strain,

as are most old

_laboratory

strains. The Canton-S and Harwich strains are M and P

type

reference

_strains,

_respectively

_(Kidwell

et

_al,

_1977).

Selection

The trait selected was the

_weight

of 2-d-old adults since

Drosophila

attains its

maximum

_weight

in 2

_days.

Cultures were maintained at a constant

_temperature

of

25°C,

with 12-h

_photoperiod,

on medium without live

_yeast

(David, 1959).

This medium was chosen because it _gave

_{good repeatability}

of

_weight

measures.

Dysgenic

D

₍₃₀

MR x 30 PI

₎

and

_nondysgenic

ND

₍₃₀

PI x 30 NIR

₎

crosses were set _up between Furnace Creek and Gruta. In the

following

generation

(GO),

mass selection was carried out for increased

_(H)

and decreased

_(L)

_body

_weight

with

_proportion

_15/60

of each sex in each

replicate

and direction of selection. The measured individuals were chosen

_randomly

_among the earliest to eclose. Selection was continued for 13

_generations.

In each

_line,

selection

was relaxed for 10

_{generations starting}

at

_generation

_14,

and

_body

_weight

was scored after 5

_(G18)

and 10

_(G23)

_generations

of relaxation. All selected lines were

kept

contemporary.

Two

_days

after the

_beginning

of the

_experiment,

a

_replicate

of it was

_performed.

The selected lines of the first

replicate

were denoted 1 and these of the second were denoted 2. At the end of the selection

_period

_{(generation 13),}

each selected line was studied with

_regard

to the P-M and I-R

_systems.

P

_{susceptibility}

determination

Standard

_diagnostic

tests based on

_measuring

_gonadal

_(GD)

_{sterility potential}

(Kidwell

et

_al,

₁₉₈₈₎

were used.

_Thirty

_virgin

females from each selected line were crossed to Harwich males and their

_offspring

were raised at 29°C

_{(cross A}

_*

_),

a

temperature

which is restrictive for

_gonadal

_sterility

in the P-M

_system.

GD

_sterility

was measured as follows : 50 Fl females

(2-d-old)

were dissected and their ovaries were examined.

_Dysgenic

ovaries were scored and the

_frequency

was calculated

(GD(A

*

)

sterility).

P

_activity

determination

P-induced GD

_sterility

Thirty

males from each selected line were crossed to 30

_virgin

Canton-S females

Hypermutability

of the

_P(t!)9.3

_composite

transposon

The

_{P(’«/!)9.3}

is a

_composite

transposon which carries the wlaite gene as a selectable

marker,

inserted within a defective P element. It can be nrobilized in trans

by

a

complete

P element

_{(Coen, 1990).}

_Forty

males from each selected line were crossed

to 40 females of the

W

i

l

l

S

_)9.3

_p

_dl

_(w

strain at 20°C. This M strain _possesses a deletion at the white locus and has been transformed

by

the

_composite

_transposon

P( w

dl

)9.3,

which is located at 19DE on the X chromosome. At the

following

generation,

40 males were

_individually

crossed to attached-X females

_lacking

P elements. The male _progeny were screened for _eye color mutants

_{(non-wild males).}

Hypermutability

was estimated

by

the mutation rate _per

_gamete,

calculated as the

weighted

average number of mutants per male. Its variance was calculated

_following

the method of

Engels

(1979).

Molecular

_analysis

In situ

hybridization

The number of P and I elements in each selected line was determined

_by

in situ

hybridization. Polytene

chromosomes from

salivary glands

were

prepared by

the

method described

by

Pardue and Gall

_(1975),

revised

_by

Strobel et al

_(1979).

Nick-translated

_px25.

_plasmid

DNA

_(O’Hare

and

_Rubin,

₁₉₈₃₎

and

_pI407

_plasmid

DNA

(Bucheton

et

al,

1984)

were used as

_probes.

For each selected

line,

2 or 3 slides were studied and a minimum of 4 nuclei per slide were examined.

Southern blots

The structure of P elements in each selected line was

_analysed

_using

the South-ern blot method. Genomic DNA was extracted

_using

the method described

_by

Junakovi6 et al

_(1984).

Restriction enzyme

digestion

of about 3 jig of DNA was

performed

according

to the

_supplier’s

instructions. After

_gel

_{electrophoresis,}

trans-fers were carried out on

_nylon

filters

_(Biodyne,

_Pall)

which were submitted to

hybridization.

The filters were

_hybridized

as recommended

_by

the

_suppliers

and

autoradiographed

using

Kodak XAR film. The Southern blots were

_hybridized

with nick-translated almost

_complete

P element from the

_prr25.7

BWC clone

_(O’Hare,

personal

communication).

RESULTS

Response

to selection

The evolution of the mean and the variance of

_body

weight

in each sex is shown

in

_figures

1 and

_2,

_{respectively,}

for the

_dysgenic

and

_nondysgenic

selected lines. For both _sexes, a

_larger

_average

_divergence

between lines selected in

_opposite

directions was observed when the

original

cross was

dysgenic,

as shown

by

the

corresponding

analyses

of variance

_(table

_I).

_However,

the

_phenotypic

variance of the lines

_(dysgenic

and

_nondysgenic)

did not

_{substantially}

_change

in the course of

For each

_pair

of

_divergent

selection

lines,

the average response

(m)

per

generation

of selection was estimated

_by

the

_regression

coefficient of the mean on

_generation

number,

and the observed response to selection

(Ro)

was estimated as 12 m.

The

_expected

response to selection

_(Re

_l3

₎

and its variance

_V(Re)

were estimated

following

the method described

_{by Pignatelli}

and

_Mackay

_(1989).

The

_expected

response to _{selection per}

_generation

is the standard Re =

ih

2

(Vp)

1/2

(Falconer,

1981),

where i is 1.3 for 15 selected from 60 of each _sex,

h

2

and

_Vp

are the realized

_heritability

and the

_phenotypic

variance

_{respectively.}

Realised

_heritability

h

2

was

estimated for each sex from

_regression

of cumulated response on cumulated selection differential over the 3 first

_generations

(Gl

to

_G3),

all

_replicates

and directions of selection were

_pooled.

The mean of the 4

h

2

estimated was the used value. For females and males from

_dysgenic

crosses

h

2

were 0.2153 and

0.0232,

respectively,

for females and males from

_nondysgenic

crosses

h

2

were 0.2233 and

0.1410,

respectively.

The estimate of

_phenotypic

variance

_(Vp)

used for each selected line was that from

_{generation 0, pooled}

over the 2

_replicates.

The

predicted

cumulated _response at

_generation

13

_(Re

_l3

₎

is then

_{l2Re, assuming}

h

2

2

and

_Vp

are constant. The

expected

variance of response from drift and

sampling

is

approximately :

2F

t

Va+(Vp

t

-(Va

t/

2))/M

(Hill, 1977),

where F

t

is the inbreeding

coefficient at time

_t,

Va is the additive

_genetic

variance

_segregating

in the base

population, Vp

t

and

_Va

_t

are the

_phenotypic

and

_{genetic variances,}

_{respectively,}

of a

_particular

selection line at time

_t,

and M is the number of individuals scored _per line each

_generation.

For lines maintained with 15

_pairs

of

_parents

per

generation,

F

(Crow. 1954).

Va was estimated from

h

2

Vp,

and

Vp

and Va were assumed to remain

_roughly

constant over 13

generations,

in the absence of mutation.

The results are shown in table II. The mean _{response per}

_generation

of selection

(rn)

is,

on _{average, 1.26} times

_greater

for the

dysgenic

than for the

_nondysgenic

selection lines. The observed _response to selection

_(Ro)

is two times

_greater

for the

light

lines than for the

_heavy

lines in males from

_dysgenic

crosses and in females from

_nondysgenic

crosses. In the other cases the _response to selection is

_symmetrical.

These data differ from

_previous

results on selection for

body

weight

(Higuet, 1986),

where the response to selection

_always

was

_greater

for

upward

selection lines. The

comparison

of the observed response

(Ro)

with the

expected

response

(Re

r3

)

shows

that in males from

_dysgenic

crosses the observed _response exceeds that

_expected

by

a factor of

_8,

whereas in males from

_nondysgenic

crosses observed and

expected

responses agree

moderately

well. In females the observed and

_expected

responses do not differ

_excepted

in females from the

_nondysgenic

_heavy

lines where the observed response

is,

on _average two times smaller than that

_expected.

_Finally,

the variance

of observed response is

greater

than the variance of the

_expected

_response and

specially

in the

_dysgenic

lines

_{(table II).}

Relaxation of selection resulted in

_decreasing

the mean

_body

_weight

of the

_heavy

lines and

_increasing

that of the

_light

lines,

for both

_types

of

_original

crosses

_(dysgenic

or

_{nondysgenic).}

After 10

_generations

of relaxation the

_divergences

between the

heavy

line and the

_light

line in the 2

_types

of

_original

crosses were not

_{significantly}

different

_{(table I).}

These results

_suggest

that some P and 1-induced mutations have a deleterious effect on fitness in the

homozygotes,

as shown

_{by Fitzpatrick}

and Sved

₍₁₉₈₆₎

and

by

1-Iackay

(1986)

and have an effect on

body weight,

so that

_{heterozygotes}

would be retained

_during

the selection _process.

In order to look for

_{relationships}

between the response to selection and the

transposition

of P and I

_elements,

_genetic

and molecular

_analyses

of the selected lines were

_performed

at the end of the selection _process

_(G13).

P

_{susceptibility}

and P

_activity

Table III shows the results of P

_{susceptibility}

and P

_{activity analyses}

carried out

at the end of the selection

_period

_(G13).

There were no differences between the 2

types

of

_original

crosses both for P

_{susceptibility}

and P

_activity,

as measured

by

GD

_sterility.

One line from the

_{original nondysgenic}

cross is a M’

_type

line

(ND2H).

This property

probably developed

during

the selection _process, due to

_genetic

drift

leading

to the loss of

P-cytotype

determinants. The P

_activity,

measured

by

the

hypermutability

of the

_P(w

_d

_{l )9.3}

_transposon,

has a

_tendency

to be

_greater

in

nondysgenic

lines than in

_dysgenic

lines.

_However,

the measure of

_{hypermutability}

does not

_{significantly}

differ between the 2

_original

crosses

(Mann

and

Whitney

U statistic not

_significant;

U =

3).

The P

_properties

of the selected lines _are

In our

_experiment

_{hypermutability}

of the

P(!!)9.3

_transposon

and

_ability

of P elements to induce GD

_sterility

are 2

practically independent

indicators of

hybrid

dysgenesis

(Spearman’s

rank correlation rs =

0.02).

This result is _not

_surprising,

since Kocur et al

₍₁₉₈₆₎

and Simmons

₍₁₉₈₇₎

_suggested

that P-induced GD

_sterility

and

_{hypermutability}

at the sn locus were also uncorrelated.

As

_expected

_(Picard,

_1976;

P61isson and

_Br6gliano,

_1987),

all selected lines were found to be inducer lines in the IR

_system.

Molecula.r

_analysis

In situ

_{hybridization}

was

performed

in order to detect

_{transposition,}

_{by comparing}

the sites in the selected lines and the Furnace Creek

_population.

The aim was to

find sites associated with selection _response.

_However,

this search was unsuccessful. A

_possible

reason for this failure was that the Furnace Creek

population

was

polymorphic

for sites of

_insertion,

many of them

being

at low

_{frequencies. Thus,}

it will be _very difficult to detect

transposition

events,

and to discriminate between drift or selection as

_causing

sites to achieve

_{high frequency. Thereby, only}

data for the mean copy number of P and I elements per

diploid

genome is

given

for each

selected line

_(table

_III).

No correlation was found between the mean number of

transposable

elements

_(P

or

I)

and the

original

cross

_type

or direction or selection. The presence of

_complete

P elements

_(able

to

_produce

_{P-transposase)}

and of P element deletion

derivatives,

in

particular

the KP element

_(Black

et

al, 1988;

Boussy

et

_al,

₁₉₈₈₎

was studied

_using

Southern blot

_analysis.

The KP element has been found _{to repress} P

_activity

when

_present

at a

_{high frequency}

_(Jackson

et

al,

1988),

thus

_repressing

eventual P-induced

_variability.

DNA was

digested

with the AvaII or DdeI _{restriction enzymes.}

_Complete

P elements and KP elements

_give

specific

restriction

_fragments

with these two enzymes

(Anxolab6h6re

et

_{al, 1990;}

Bi6mont et

_al,

_1990).

All selected lines possess the

complete

P element and the KP

element

_{(table III),}

_except

one

(ND1L)

_lacking

a KP element. No other

_particular

deletion derivative element was found to be associated with the

type

of cross or direction of selection.

DISCUSSION

In our

_experiment,

as in

_{Mackay’s experiment}

(1985),

a

_greater

response to selection was found when the

_original

cross was

_dysgenic

than when it was non

_dysgenic.

But

in our case the difference between

_dysgenic

and

_nondysgenic

crosses was weaker than

previously reported

(Mackay, 1985).

The response to selection in our

_dysgenic

cross

was 1.26 times

_greater

than in the

_nondysgenic

cross when it was twice in

_Mackay’s

experiment.

Moreover,

the

_phenotypic

variances of

_{body weight}

of the selected lines did not differ between the 2 cross

_types,

in contrast to

_Mackay’s

data on abdominal bristle number. It is

_possible

that the reason of this

_discrepancy

could be attributed to the choice of the P strain. The Furnace Creek strain used in our

_experiment

is

Furnace Creek.

_{Thus, transposition}

rate and its consequence could be

greater

in

iVIackay’s

experiment

than in our own.

In our

_experiment,

the response to selection of lines started from the

_dysgenic

cross was

_larger

than that from the

_nondysgenic.

_However,

the

_relationship

be-tween this result and

_{transposition}

events remains unclear.

Here,

as in

Mackay’s

experiments

(1985),

the

_difficulty

of

_associating

events of

_{transposition}

and their

consequences with the response to selection is due to the

_experimental

method used.

Mackay

(1986),

Torkamanzehi et al

_(1988),

and

_Pignatelli

and

_Mackay

₍₁₉₈₉₎

have inferred that

_{transpositions}

occur in

_nondysgenic

lines. More

_{recently Shrimpton}

et al

_(1990),

_using

in sitv,

_{hybridization}

in lines selected for abdominal bristle

_by

Mackay

(1985),

found no difference in total number of sites per

_line,

mean number

of sites per

individual,

mean _{copy number per}

_individual,

or site

_frequency,

between

dysgenic

and

_nondysgenic

selected

_lines,

nor between lines selected in

_opposite

di-rections.

_Therefore,

it is not

_surprising

not to find _any difference in the mean _copy number of P and I elements or in the nature _{of the P elements between the genomes} of selected lines started from the 2 cross

_types.

Because

_{transpositions}

and their consequences occur in

nondysgenic

as well as in

_dysgenic

crosses, the former cannot be used as a control or

_only

in the first

_generations

₍₅

_generations

after the

_original

_cross),

after which

_dysgenic

and

nondysgenic

crosses become similar in

regard

to the

_{transposition}

rate. To cope

with the

_problem

of control of the

_{transposition,}

Lai and

_Mackay

₍₁₉₉₀₎

propose a different

_{approach :}

to determine the

_ability

of the P-M

_{hybrid dysgenesis}

_system

to

_generate

mutations

_affecting

bristle number

_they

construct X chromosome lines in which X chromosomes were

_exposed

to a

_dysgenic

cross and a

_nondysgenic

cross and recovered in common autosomal

backgrounds. They

show that

dysgenic

crosses are 3 times more effective than

_nondysgenic

crosses in

_{inducing polygenic}

variation. The new variation

_resulting

from one

_generation

of

_mutagenesis

has

_large

effects on bristle score, and all mutations reduced bristle number. Other

types

of

_experiments

have been

_performed

related to

_ascertaining

the effect of

_transposable

elements on fitness

_(for

review see

Mackay,

1989),

in

particular experiments using

a controlled

source of

_transposase.

Finally,

another

_parameter

must be considered. Several studies

_(Williams

et

al,

1988;

Robertson and

_Engels,

1989;

Coen,

1990)

imply

that

_{repressor-making}

mutant P elements affect the

_expression

of P insertion mutations. Thus the response

to selection could be due to P-induced mutations and could be

_{cytotype-dependent}

owing

to the

_expression

of

_{cytotype-dependent}

P insertion mutations.

ACKNOWLEDGMENTS

REFERENCES

Anxolabéhère

D,

Hu

K,

Nouaud

D, P6riquet

G

₍₁₉₉₀₎

The distribution of the P-M

system

in

_{Dro.sophila rnelanogaster}

strains from the

People’s

Republic

of China. Genet Sel

_{Evol 22,}

175-188

Bi6mont

C,

Ronsseray

S,

Anxolab6h6re

_D,

Izaabel

_H,

Gautier G

₍₁₉₉₀₎

Localization of P

elements,

copy number

regulation,

and

cytotype

determination in

_Drosophila

melanogaster.

Genet Res

_(Camb)

_56,

3-14

Black

_DIVI,

Jackson

_MS,

Kidwell

_1BMG,

Dover GA

₍₁₉₈₈₎

_{KP elements repress} P-induced

_hybrid

_dysgenesis

in D

_{rraelanogaster.}

EMBO

_{J 6,}

4125-4135

Bregliano JC,

Kidwell MG

₍₁₉₈₃₎

_Hybrid

_dysgenesis

determinants. In : Mobile Genetic Elements

_(Shapiro

_{JA, ed)}

Academic

_{Press, NY,}

363-410

Boussy IA, Healy !MJ,

Oakeshott

_JG,

Kidwell MG

₍₁₉₈₈₎

Molecular

_analysis

of the P-1!T

_{gonadal dysgenesis}

cline in Eastern Australian

Drosophila

melanogaster.

Genetics

_119,

889-902

Bucheton

A,

Paro

R,

Sang

HM,

Pelisson

A,

Finnegan

DJ

₍₁₉₈₄₎

The molecular basis of I-R

_{hybrid dysgenesis}

in

_{Drosophila melanogaster : identification,}

_cloning

and

_properties

of the I factor. Cell

_38,

153-163

Coen D

₍₁₉₉₀₎

P element

_regulatory

_products

enhance

zeste

l

repression

of a

P(white duplicated )

transgene

in

_{Drosophila melanogaster.}

Genetics

_126,

949-960 Crow JF

₍₁₉₅₄₎

_Breeding

structure of

_populations.

II. Effective

_population

number. 7n : Statistics and Mathematics in

_Biology.

Iowa State Coll

Press,

Ames, IA,

543-556 David JR

₍₁₉₅₉₎

Etude

_quantitative

du

_{d6veloppement}

de la

_Drosophile

6lev6e en milieu

_ax6niqtie.

Bull Biol Fr Bel

_93,

472-505

Engels

WR

₍₁₉₇₉₎

The estimation of mutation rates when

_premeiotic

events are involved. Environ

_Mutagen

_1,

37-43

Engels

V’R

₍₁₉₈₃₎

The P

_family

of

_transposable

elements in

_Drosophila.

Ann Rev Genet

_17,

315-344

Engels

WR.

₍₁₉₈₈₎

P elements in

_Drosophila.

In : Mobile DNA

_(Berg

_D,

Howe

_M,

eds)

ASNI

_{Publications,}

_Washington,

_DC,

437-484

Falconer DS

₍₁₉₈₁₎

Introduction to

_Quantitative

Genetics.

_Longman,

London

Finnegan

DJ

₍₁₉₈₉₎

The I factor and I-R

hybrid

dysgenesis

in

_Drosophila

raelanogaster.

In : Mobile DNA

_(Berg

_D,

Howe

_M,

_eds)

ASM

_{Publications,}

Wash-ington, DC,

503-518

Fitzpatrick

BJ,

Sved JA

₍₁₉₈₆₎

_High

levels of fitness modifiers induced

_{by hybrid}

dysgenesis

in

_{Drosophila T}

_{nelanogaster.}

Genet Res

48,

89-94

Gvozdev

_{VA, Belyaeva ES, Illyin}

_YV,

Amosova

_IS,

Kaidanov LZ

₍₁₉₈₁₎

Selection and

_{transposition}

of mobile

_dispersed

_{genes in}

_{Drosophila rrtelanogaster.}

Cold

_Spring

Harbor

_Symp

Quant

Biol

_45,

673-685

Higuet

D

₍₁₉₈₆₎

_Disruptive

selection on

_{body weight}

in

_Drosophila

melanogaster.

Evolution 40

_(2),

272-278

Hill WG

₍₁₉₇₇₎

Variation in response to selection. In : Proc Int

_{Conf Quant}

Genet

(Pollack

E, Kempthorne 0, Bailey TB,

eds)

Iowa State

_University

Press,

Ames, IA,

343-365

Junakovic

N,

Caneva

_R,

Ballario P

₍₁₉₈₄₎

Genomic

distribution

of

_copia-like

element in

_laboratory

stocks of

_Drosophila

_{melanogaster.}

Chromosoma

_90,

378-382 Kidwell

_MG,

Kimura

K,

Black DM

₍₁₉₈₈₎

Evolution

of

_hybrid

_{dysgenesis potential}

following

P element contamination in

_Drosophila

_{melanogaster.}

Genetics

_119,

815-828

Kidwell

_MG,

Kidwell

JF,

Sved JA

₍₁₉₇₇₎

_Hybrid

_dysgenesis

in

_Drosophila

melanogaster.

A

_syndrome

of aberrant traits

_including

_mutation,

_sterility,

and male recombination. Genetics

_86,

813-833

Kocur

_GJ,

Drier

_EA,

Simmons MJ

₍₁₉₈₆₎

_Sterility

and

_{hypermutability}

in the PM

system

of

_hybrid

_dysgenesis

in

_{Drosophila melanogaster.}

Genetics

_114,

1147-1163 Lai

_{C, Mackay}

TFC

₍₁₉₉₀₎

Hybrid

dysgenesis-induced

quantitative

variation on the X chromosome of

_Drosophila

_{melanogaster.}

Genetics

_124,

627-636

Mackay

TFC

₍₁₉₈₄₎

_Jumping

genes meet abdominal bristles :

_hybrid

dysgenesis-induced

_quantitative

variation in

_{Drosophila melanogaster.}

Genet Res

_44,

231-237

Mackay

TFC

₍₁₉₈₅₎

_Transposable

_{element-induced response} to artificial

selection

in

_{Drosophila mela!aogaster.}

Genetics

_111,

351-374

Mackay

TFC

₍₁₉₈₆₎

Transposable

elements induced fitness mutations in

_Drosophila

melanogaster.

Genet Res

_48,

77-87

Nlackay

TFC

₍₁₉₈₉₎

_Transposable

elements and fitness in

_Drosophila.

Genome

_31,

284-295

Morton

_RA,

Hall SC

₍₁₉₈₅₎

_Response

_{of dysgenic}

and

_non-dysgenic

_populations

to

malathion exposure.

Drosophila Inf

Serv

61,

126-128

O’Hare

K,

Rubin G1!T

₍₁₉₈₃₎

Structure of P

_transposable

elements and their sites of insertion and excision in the

_{Drosophila melanogaster}

genome.

Cell

34,

25-35 Pardue

ML,

Gall JG

₍₁₉₇₅₎

Nucleic acid

_{hybridization}

to the DNA of

_cytological

preparation.

In : Methods in Cell

_Biology

_(Prescott

DM,

ed)

Academic

_{Press, NY,}

1-16

P61isson

_{A, Br6gliano}

JC

₍₁₉₈₇₎

Evidence for

_rapid

limitation of the I element copy

number in a _genome submitted to several

_generations

of IR

_{hybrid dysgenesis}

in

Drosophila melanogaster.

Mol Gen Genet

207,

306-313

Picard G

₍₁₉₇₆₎

Non-Mendelian female

_sterility

in

_{Drosophila melanogaster :}

hereditary

transmission of I factor. Genetics

83,

107-123

Pignatelli

PM,

Mackay

TFC

₍₁₉₈₉₎

_{Hybrid dysgenesis-induced}

_response to selection

in

_Drosophila

_{melanogaster.}

Genet Res

54,

183-195

Robertson

HM,

Engels

WR

₍₁₉₈₉₎

Modified P elements that mimic the P

_cytotype

in

_Drosophila

_{melanogaster.}

Genetics

_123,

815-824

Shrimpton AE,

Mackay

TFC,

Leigh

Brown AJ

₍₁₉₉₀₎

_Transposable

element-induced _response to artificial selection in

_{Drosophila melanogaster :}

molecular

analysis

of selection lines.

Genetics

125,

803-811

Simmons

GM

₍₁₉₈₇₎

Sterility-mutability

correlation. Genet Res

50, 73-76

Strobel

_E,

Dunsmuir

_P,

Rubin

GM

₍₁₉₇₉₎

_Polymorphism

in the chromosomal locations of the

_{412, copia}

and 297

_{dispersed repeated}

gene families in

Drosophila.

Torkamanzehi

A,

Moran

C,

Nicholas FW

₍₁₉₈₈₎

P-element-induced mutation and

quantitative

variation in

_{Drosophila rrcelanogaster :}

lack of enhanced response to selection in lines derived from

_dysgenic

crosses. Genet Res

_51,

231-238