"Cut-bristles" : a sex-limited mutant phenotype of male orbital bristles of Ceratitis capitata

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”Cut-bristles” : a sex-limited mutant phenotype of male

orbital bristles of Ceratitis capitata

C Lemaitre, Jp Carante

To cite this version:

Note

"Cut-bristles" :

a

sex-limited

mutant

_phenotype

of male orbital

bristles

of

Ceratitis

_capitata

C

Lemaitre,

JP

Carante

Université C

_{Bernard, Lyon}

1 et Institut U!aiversitaire de

_{Technologie A,}

URA 243 Biométrie,

Génétique

et

_Biologie

des

_Populations,

43 Bd du 11 7Vo!em6re _1918, 696!2 _{Villeurbanne,} France

(Received

15

_July

_1991;

_accepted

15

_May

₁₉₉₂₎

Summary - The "cut-bristles"

_phenotype,

a new mutant of Ceratitis capitata, is charac-terised

_by

the

_{disappearance}

of the

_lancet-shape

bristles, a male sex-limited trait. This mutation seems to be under the control of 2

_major

recessive _genes,

_probably

with several additional minor _ones, which account for

_incomplete

and variable _penetrance. Two models are

_compatible

with our data: 2 autosomal syntenic, but distant genes

(no

recombination in

_males)

or 1 sex-linked and another autosomal gene.

Mediterranean fruit _fly

_/

Ceratitis capitata

/

"cut-bristles" mutant

Résumé - _{Étude génétique} d’une mutation morphologique de Ceratitis capitata: «cut-bristles». Le

_phénotype

«cut-bristles»

_correspond

à la

disparition

des soies orbitales en

forme

de

_lance,

attributs

_{caractéristiques}

du sexe mâle. Ce

_phénotype

se révèle être sous le contrôle de 2

_gènes

_majeurs

_récessifs

et sans doute de

_plusieurs

autres

_gènes

_mineurs,

permettant

d’expliquer

la

_pénétrance

variable et

_incomplète

observée _pour ce caractère. Deux modèles sont

_compatibles

avec nos rés.ultat.s:

_{2 gènes}

autosorrziques,

synténiques

mais

éloignés

l’un de l’autre

_(pas

de recombinaison chez le

₇

_nâle)

ou un

_gène

lié au sexe et un autre autosomique.

INTRODUCTION

Over the past

decade, genetic knowledge

of the

_medfly

increased

_rapidly

as the need

for

_pest

control programs was

_recognized

_(see

_Saul,

_1986,

for

_review).

There are,

however,

still

_only

few

_genetically

marked strains available for

_ecological

studies,

and the list established

_by

R6ssler

₍₁₉₈₉₎

constitutes a _poor set

_compared

with other

pests.

It is thus _necessary to consider _any kind of

_{morphological}

mutants,

even if their mode of inheritance is still unclear.

Four orbital bristle mutants are mentioned in the

literature,

but

only

2 of

them have been

_analyzed.

The first

mutation,

found

_by

Cavicchi

_(1973),

involved chaetae

_shape

and stem colour and was

_recessive,

_monogenic

and autosomal. The

second mutant,

&dquo;double-chaetae&dquo;,

isolated

_by

R6ssler and Koltin

₍₁₉₇₆₎

concerned the number of

bristles;

its

_underlying

_genetic

_system

was not clear and did not

conform well to the

_segregation

ratios

_expected

from a

_single

_gene model. From

further

studies,

this deviation was attributed to

_incomplete

_penetrance

and variable

expressivity

of the character

_(R6ssler,

_1982a;

Saul and

R6ssler,

1984).

Here we

present an additional

_{morphological}

mutation we named &dquo;cut-bristles&dquo; . This variant concerns the characteristic lancet

shape

bristles of Ceratitis

capitata males,

an

ornament described as ‘‘subarticulate

horns,

planted

between the

eyes...&dquo; by

Mac

Leay

(1829).

MATERIALS AND METHODS

We used 2 strains: a wild

strain,

donated

by

a French

laboratory

in 1968

(Avignon)

and a mutant

_strain,

isolated from another strain

_(inbred

because of a selection

carried out on a nutritional criterion 1 _year

ago)

itself

originated

from a strain

(Antibes)

kept

in the

_laboratory

since 1978. Both had been

_caught

in

_Tunisia,

but

at different

_geographical

sites and times. These strains were reared under

_laboratory

conditions for several years

(see

Carante and

Lemaitre,

1990 for

rearing

conditions).

Virgin

females were isolated in

_separate

containers within 24 h of _emergence,

and were mated within the

_following

5 d. For transfer and

_scoring

adults were

immobilized

by

chilling

at 10°C.

In each cross, the flies were mated

(at

least 5

_pairs

of

flies)

or in

single

_pairs

(single

pairs

were

_always

less fecund than mass-mated flies and were often

_sterile).

Two

_repetitions

were carried _out, and their

results,

found not to be

_{statistically}

different

_{by x2 test,}

were

_pooled.

RESULTS AND DISCUSSION

Description

of the

_phenotype

The &dquo;cut-bristles&dquo; trait

_corresponds

to the absence of anterior frontal orbital

bristles,

exactly

as if

they

were cut at their base shaft. Some males bear

_only

one

1980 and

Lifschitz,

1985)

which are

_simply

mentioned as autosomal

incomplete

dominant

_traits,

without _any

_analysis.

The &dquo;cut-bristles&dquo;

_trait,

or even a

_simple

_{shape change}

of the

_analogous

bristles,

has never been observed in

females;

the

genetic

analysis

was thus based

_only

on

the male progeny

phenotypes.

Dissection of

_pharate

adult

_puparia

1

_day

before emergence showed that the

orbital bristles of &dquo;cut-bristles&dquo; males were

_normally

formed but

_unpigmented,

contrary

to those of wild males. When a &dquo;cut-bristles&dquo; male was removed from its

nymphal wrapping,

the bristle shaft broke most of the

_time;

this never

happened

with wild males. The mutant

_{phenotype, therefore,}

came from the break of the

orbital bristle shaft at emergence time because of its brittleness.

Selection and establisment of a &dquo;cut-bristles&dquo; strain

The first &dquo;cut-bristles&dquo; male was found in

_1980,

in an inbred line. This male was

mated to its

_sisters,

&dquo;cut-bristles&dquo; males were sib-crossed each

_generation,

and a

&dquo;cut-bristles&dquo; strain was established from that time. The fraction of &dquo;cut-bristles&dquo;

males reached its maximum

_(ie

_92%)

within 6

_generations,

but the selection pressure was maintained until the 17th

_generation

before

being stopped.

This relaxation of

generations,

so we considered our selected strain as a

_{true-breeding}

one.

Despite

the

fact that mutant females were

_{indistinguishable}

from

_wild-type,

we assumed that

females of the selected strain were of mutant

_genotype,

and

_they

will be referred to as &dquo;rnutant females’’ in the text.

The

_persistence

of a few

_wild-type

(about 2% )

and uni-bristle

_type

(about 6% )

males

_throughout

the

_generations

of selection is troublesome. It demonstrates some

variability

in the

_expression

and

_penetrance

of the

_phenotype.

No &dquo;uni-bristle&dquo; male has ever been found in the wild strain. Inheritance of the &dquo;cut-bristles&dquo; trait

Male and female mutants were crossed to the

_wild-type

_laboratory

strain

(Avi-gnon).

These crosses

_{yielded wild-type}

_progeny, with a _very small

_proportion

of

males with 1 or 0 bristle

_(table

_I).

The mutation is thus _{recessive. The appearance} of a few mutants _may result either from the presence of individuals

heterozygous

for the mutation in the wild

_strain,

from

_non-virgin

mutant

_females,

or the occur-rence of

_{phenocopies resulting}

from

_particular

environmental conditions. To check some of these

points

the uni-bristle

F

l

males were

pair-mated

to

_virgin

&dquo;mutant

females&dquo;. These crosses

_produced

85

_wild-type,

38 uni-bristle and 144 cut-bristles

males. This

_phenotypic

distribution was similar to that

_{produced by}

the

_F

_l

wild-type

males crossed with &dquo;mutant females&dquo;

_(F

_2am

and

_F

_2n

_&dquo;,

in table

I ;

X

2

=

_6.13,

_for

genotype

as

_F

₁

wild

_type

males.

_Consequently

we

_postulate

that

_they

were het-erozygous for the studied

genetic

system; the

_frequencies

of these 2

_phenotypes

were therefore

pooled

in statistical

_analyses.

The fact that the same

_genotype

can

lead to different

_phenotypes

means that the wild

_type

allele involved was

incom-pletely

dominant.

The

_phenotypic

distribution of the

_progenies

of F

l

sib-crosses

_(F

_2aa

and

_F

_2bb

and

F,

reciprocal

test-crosses

_(F

_2am

and

_F

_zbm

and

_a

_&dquo;,

_z

_F

and

_F

₂

_&dquo;,

_b

₎

are not consistent

with a

_single

locus model.

_Moreover,

the test-crosses

_yielded

_segregation

ratios

which differed

according

to the sex of the

heterozygous

_parent.

We consider that

the

_genetic

_system

was thus either

_sex-linked,

or at least

_partly

sex influenced.

Reciprocal homologous

crosses

_{yielded statistically}

similar _progeny distributions

(see

k

2

in table

_I),

and the ratio values of &dquo;cut-bristles&dquo; males to males with 1 and

2 bristles

_suggest

a 2-loci model for the

_genetic

control of the mutation.

According

to Carante’s

_proposals

₍₁₉₈₃₎

these 2 loci can be

_{symbolized by}

obn2

and obn3

_(from

orbital

_number)

and the

_respective

mutant and wild

_type

alleles

_by

obn2(ct), obn2(

+

)

and

_{obn3(br), obn3(+);}

for

brevity,

we will use

only

ct, br or +

(the

parenthetical

part

of the locus

_symbols),

so the

following

allelic associations

(+,+), (ct,+)

and

_(+,br)

_correspond

to the wild

_phenotype

and

_(ct,br)

to the

mutant one.

Two models are

_compatible

with the results:

Model 1: 2 autosomal loci

According

to the

_F

_la

and

_F

_ib

_progenies,

the 2 loci are

closely linked,

but

according

to the

_F

_2ma

and

_F

₂

_,n

_b

_progenies

the 2 loci are

_independent.

To resolve this

discrepancy

we

_postulate

that:

₁₎

the 2 loci

_belong

to the same

_syntenic

_group;

2)

they

are far

_enough

from each other to

_yield

a recombination level in females so

high

as to seem

_independent;

3)

the recombination level _{is very} low in males as in some other

_{Dipteran species.}

According

to this

_hypothesis,

all the

_F

_l

_genotypes are

_similar,

whatever the

direc-tion of the cross. The mean

frequency

value of

F

2

&dquo;,

a

and

F

2mb

&dquo;cut-bristles&dquo; males is 0.26. These males occur from 1 of the 2 non-recombinant female

_gamete-types

produced

by heterozygous

F,

females. We _may thus assume a non-recombination level of 0.52

_(and

therefore a recombination level of

0.48)

in females. This

_high

value indicates that the 2 loci are _{very distant.} Accurate location would need

fur-ther studies

_using

intermediate markers. The mean

_frequency

of

_F

_2am

and

_F

_2bn

_,

&dquo;cut-bristles&dquo; males is 0.46. These males occur from non-recombinant

_gametes

pro-vided

_{by heterozygous}

_F

₁

males. We estimate the recombination level to be 0.04 in

males. Such values conform with

_previous

estimates of Robinson and Van Heemert

(1982),

R6ssler

_{(1982a,b; 1985)}

and R6ssler and Rosenthal

_(1988).

The

_frequency

of

F

2aa

and

_F

_2bb

&dquo;cut-bristles&dquo;

_males,

_resulting

from 2 non-recombinant

_F,

_parental

gametes

would then be

equal

to 0.125. This

expected

value is not

_{statistically}

dif-ferent from the observed results

_(0.110

for

_F

₂

_{,. :}

_X

₂

=

_3.594,

1

_df,

P _{> 0.05 and}

Model 2: one sex-linked and one autosomal loci

In

medfly

the female sex is

homogametic

and the male is

heterogametic

(Radu

et

_{al, 1975; Saul, 1985;}

Lifschitz and

Cladera,

1989).

All the

F,

males were thus

heterozygous

for the autosomal

locus,

but

_they

differed in the allelic form borne

by

the X-chromosome:

F

la

males

_presented

the wild form and the

F

lb

males the

mutant one. The similar

_phenotypic

distributions of these 2

F,

males

(see

table I:

x

2

=

0188,

1

df,

P _>

0.05),

_suggest

that the 2 alleles involved acted in a similar way and had no additive action _upon the trait.

At the

F

2

generation,

the

genotypes

of the

_offspring

_{depend only}

on the

_mating

type,

and the

_expected

value of the &dquo;cut-bristles’’ male relative

frequency

is

_1/2

for

_2am

_F

and

_F

_Zb,r&dquo;

₁

_/

₄

for

_F2&dquo;,a

and

_mb,

_F

₂

_1/8

for

_F

₂

_aa

and

F

2bb

.

The observed results are consistent with these

expected

values

(x

2

=

0.467, 0.500,

0.012, 1.026,

3 .

594 and 0.345 for

_{F2am! F}

_2b

_m,

_F

_2ma

_,

_.

_2mb

_F

F

2aa

;

and

F

2bb

,

respectively,

with 1

df

and P >

_0.05).

Like R6ssler and Koltin

₍₁₉₇₆₎

with their double chaetae

_mutation,

we were

confronted in our

_analyses

with the

_{imperfect correspondence}

between

_phenotypes

and

_genotypes.

F

1

&dquo;uni-bristle&dquo; males

_{incontestably}

behave like

F

1

wild

type

males when

_they

are crossed with &dquo;cut-bristle&dquo;

_{females; however,}

when

_persistent

&dquo;uni-bristle&dquo; males of the selected strain are

_equally

crossed with their

_sisters,

_{they yield}

a

progeny similar to that of &dquo;cut-bristles&dquo; males. This

_ambiguity,

which would

require

particular study,

could be

_imputed

to

_modifying

minor _genes, whose association is removed

throughout

the

_selection,

_interfering

with

major

gene

expressivity.

Beside the 2

_major

_genes involved in the

_genetic

determinism of the &dquo;cut-bristles&dquo;

phenotype,

we must thus consider minor ones, scattered

throughout

the chromosomes.

_They

may account for

_incomplete

penetrance

and variable

expressivity

of this

trait,

as well as

_incomplete

dominance of

_wild-type

of

_F

₁

males.

To set _{up any}

_population

_biology

or

ecology

study,

markers are essential. At

present

a maximum of 38 adult

morphological

mutants of Ceratitis

_capitata

are

known,

a number which is _very

_likely

much smaller because of the

high degree

of

redundancy

among them

(R6ssler, 1989);

furthermore,

27 of them are color variants

whose

_{stability throughout}

time is unknown. So for such studies the

_{potential &dquo;good}

mutants&dquo; are

_probably

_very scarce and we consider that the ‘‘cut-bristle&dquo;

trait,

with its easy identification and

persistence

through

ageing

and

death,

could be an

available marker.

ACKNOWLEDGMENTS

The authors thank C Biémont for his

_judicious

advice in the

_editing

of this text and A Heizmann for her valuable technical assistance with

_breeding.

REFERENCES

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