The genetic properties of homosexual copulation behaviour in Tribolium castaneum: artificial selection

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The genetic properties of homosexual copulation

behaviour in Tribolium castaneum: artificial selection

L Castro, Ma Toro, C López-Fanjul

To cite this version:

Original

article

The

_{genetic properties}

of homosexual

copulation

behaviour in

Tribolium

castaneum:

artificial

selection

L

Castro

MA

Toro

C

_{López-Fanjul}

₂

1

Instituto Nacional de

_{Investigaciones Agrarias, Departamento}

de Producién

Animal,

Apartado

8111, 28080

_Madrid;

2

Facultad de Ciencias

Bioldgicas, Departamento

de

_Genética,

Universidad

_{Complutense, 280l,0 Madrid, Spain}

(Received

18

_January

1993;

accepted

2 December

₁₉₉₃₎

Summary - Artificial

_divergent

selection for the rate of homosexual

copulation

(defined

as the

_proportion

of homosexual

_{mountings performed by}

a male in a

period

of 30

min)

has been carried out for 2-3

_generations

in a

_population

of Tribolium castaneum. A clear response was obtained in each of 4

replicates, corresponding

to an overall realized

heritability

of 0.11 f 0.01. No

significant

correlated _response to selection was observed for the average number of

mountings performed by

a male

_during

the

_{testing period.}

Therefore,

our results do not agree with

evolutionary interpretations

of insect homosexual

copulation

behaviour based on the existence of a

_negative

_genetic

correlation between the

degree

of sexual discrimination and sexual activity. On the contrary,

they strongly

favour the

_hypothesis

of sex

_{recognition being}

absent in Tribolium casteneum.

homosexual copulation behaviour

_/

artificial selection

_/

l!ibolium castaneum

Résumé - Les _{propriétés génétiques} du comportement de _copulation homosexuelle

chez Tribolium castaneum : sélection artificielle. Une sélection

divergente

pour le taux de

copulation

homosexuelle

_(défini

comme la

_proportion

des montes homosexuelLes réalisées par un mâle sur une

_période

de 30

min)

a été réalisée sur 2-3

_{générations}

dans une

population

de Tribolium castaneum. Une

_réponse

nette a été obtenue dans chacune des

4

répétitions (1

lignée

haute et 1

_lignée

basse par

répétition),

qui

correspond

à une héritabilité réalisée de

0,11 ±

0,01. Il n’a _pas été observé de

_réponse

indirecte à la sélection en ce _qui concerne le nombre _moyen de montes réalisées par un mâle sur la

sexuelle. Au contraire, les résultats

suggèrent

très

fortement

l’absence de reconnaissance

du sexe chez ’Iribolium castaneum.

comportement de _copulation homosexuelle

_/

sélection artificielle

_/

Tribolium casta-neum

INTRODUCTION

In Tribolium castaneum and T

_confusum,

_high

rates of homosexual

_copulation

(defined

as the

proportion

of homosexual

mountings

performed by

a male in a

period

of 30

_min)

have often been

_reported

_(Wool,

_1967;

_Taylor

and

_{Sokoloff, 1971;}

Rich, 1972, 1989;

Graur and

_Wool,

_1982).

_They

have

_routinely

been considered as

’mistakes’,

or as a sort of

_pathological

behaviour

_resulting

from crowded

_laboratory

conditions.

_{Notwithstanding,}

Serrano et al

₍₁₉₉₁₎

found

_good

_agreement

between

observed rates of homosexual

copulation

in T castaneum and those

_expected,

assuming

random

_pair

contacts between

_potential

mates, when both sexes

_equally

oppose

being

mounted. This result has been shown to

apply

in a

_variety

of

experimental

situations,

indicating

that T castaneum males are indiscriminate with

respect

to sex.

The rate of homosexual

_copulation

has been shown to be

_genetically

variable in a

laboratory population

(Consejo

population),

by

means of a diallel

_analysis

of inbred

lines and their

_F

₁

crosses

(Serrano

et

_al,

_1991).

Nevertheless,

no

_attempt

was made

to

_identify

the forces

maintaining

that variation. Thornhill and Alcock

₍₁₉₈₃₎

have

proposed

an

_evolutionary

_{interpretation}

of insect homosexual

copulation

behaviour,

considered as a

by-product

of

perception

errors.

_Assuming

that the main cost of

reproduction

is the time consumed

_by

the male in

_discerning

the sex of

potential

mates,

increasing

the number of

_mountings

_per unit

_time,

at the risk of

_making

some

_mistakes,

_may be more

advantageous

than

carefully choosing

a

_partner

of the

right

sex. This

implies

the existence of a

_{positive genetic}

correlation between the

rate of homosexual

_copulation

and

_{mating activity,}

but estimates of this

parameter

are not available.

In the

_present

_work,

artificial

_divergent

selection was carried out for the rate

of homosexual

copulation

to further

_study

the

_genetic

variation of the character. In

_addition,

the

_{genetic relationship}

between homosexual

copulation

and sexual

activity

has been

_explored.

MATERIALS AND METHODS

The

_{Consejo population}

was

captured

near Madrid and has been maintained in a

cage in this

laboratory

since 1964. All lines in this

experiment

were

_kept

at

70%

relative

_humidity

and 33°C. The culture medium consisted of

95%

whole wheat flour and

5%

dried, powdered

brewer’s

_yeast.

_Pupae

were sexed

by

examination of

the

_genital

lobes. Male pupae were

kept individually

and female pupae stored at

Mating

cannot be observed within the culture medium as beetles show a

_strong

photonegative

reaction. In this

_situation,

our observations were made as follows.

Two males

_(identified

_by

a white or a

_yellow

_spot

of

_paint

on the

_thorax)

were

placed

in a

glass

vial

(3

cm diameter x 3.5 cm

height)

with a filter _paper

floor,

together

with 2

_virgin

females from the unselected base

_population.

For each

_male,

the number of homosexual and heterosexual

_mountings

were recorded

_during

30 min

on each of 5 consecutive

days,

the females

being

substituted

by

a new

_pair

each

day.

Ten such vials were observed

simultaneously. Only

those homosexual

_matings

in which the

_mounting

males showed

_symptoms

of

_{being sexually}

aroused

_(extension

of

_aedagus)

were recorded as such.

_Thus,

the rate of

homosexual

_copulation

can be

calculated for each male as the ratio between the number of homosexual

_mountings

and the total number of

_mountings

recorded

_(homo-

and

_{heterosexual).}

Divergent

selection for the rate of homosexual

_copulation

was carried out in 4

non-contemporary

replicates, although

the

_high

and low lines of the same

_replicate

were

_always

handled

simultaneously.

Individual selection was

practised

in each

line on males. In all

_lines,

the best 5 males were selected out of 40

tested,

and

individually

mated to females taken at random from the same line and

_generation

(full-sib

matings

were

_avoided).

Each

_mating

contributed 8 males and 8 females to

the next

_generation.

The mean and the coefficient of variation of the rate of homosexual

_copulation,

as

well as its

daily repeatability,

are shown in table I for the

Consejo population.

The rates of homosexual

_copulation

of males identified with either a white or

a

_yellow

_spot

of

_paint

did not

_{significantly}

differ

₍

_XI

=

0.004).

No

significant

heterogeneity

was found between observations of the

_mating

behaviour of males

during

5 consecutive

_days

₍

_X4

₌

_8.4);

a

_learning

effect can therefore be discarded in

our

_experimental

conditions. This is not

_surprising

as an

_intervening

_period

of 23 h

elapsed

between consecutive tests.

_Obviously,

this result cannot be

extrapolated

to

laboratory

or wild

_populations

where

_mountings

would occur

_{continuously.}

The average rate of homosexual

copulation plotted against generation

number

is

_presented

in

_figure

1 for the individual

_replicates.

The difference between the

performance

of the

_upward

and downward selected lines was

_{statistically}

significant

at _any

_generation

in

_all

_replicates.

On _average, a considerable

_divergence

of

11.9%

t 1.2 was obtained after

_only

2-3

_generations

of selection. These results

clearly

The response to selection was

_{approximately symmetrical}

in

_replicates

1 and

2

_(about

_6%

in each

_direction),

and

_{patently asymmetrical}

in

_replicates

3 and

4,

where much

_larger

responses

(11-13%)

were observed in the

high

line but no

response was detected in the low line. On _average, a much

_larger

_response was

attained in the

_upward

direction. After the data were arcsine transformed

(not

shown)

asymmetry

was still

_present,

_indicating

that it cannot be accounted for

by

scale effects. Overall realized heritabilities

_(standard

errors corrected for

_drift;

Hill,

1972a,b)

were 0.17 ! 0.02

_(upwards),

0.08 ±0.01

_(downwards)

and 0.11 ±0.01

(divergence).

The _average number of

_mountings

_(homo-

and

_{heterosexual)}

_{performed by}

a

male in 30 min is shown in table II for the initial and final

_generation

of selection for all lines. Male sexual

_activity

increased

_slightly

with selection.

_However,

this occurred

_irrespective

of the direction of selection and therefore this

_change

can be

better ascribed to an unidentified time trend. This is consistent with a

_higher

value

(3.68 ! 0.20)

obtained

_by

Serrano et al

₍₁₉₉₁₎

with the same base

_population.

At

the final

_generation,

no

_significant

differences were found between the male sexual

the

_genetic

correlation between this trait and the rate of homosexual

_copulation

must be small or non-existent.

The

_phenotypic

correlations between the rates of homosexual

_copulation

of

the 2 males tested

_together

in the same vial was

_negative

but

_negligible

_(-0.11;

confidence interval

_-0.05,

_-0.17).

In

_parallel,

the

_phenotypic

correlation between the average number of

mountings

in 30 min and the rate of

_{homosexuality}

of a

male was

_positive

but small

_(0.19;

confidence interval

_{0.13, 0.25).}

Both correlations have been calculated from

_pooled

data

_(base

_population

and selected

_lines).

Non-signficant

estimates of these correlations were obtained

_by

Serrano et al

_(1991).

DISCUSSION

Our

_{experimental design}

consisted of 4

_{non-contemporary}

_replicates

_but,

in each of

_them,

artificial selection was carried out in both directions on a

strictly

con-temporary

schedule.

_Thus,

the data allow us to evaluate

_correctly

total _response

(divergence)

to

selection,

either direct or correlated.

Strictly speaking, however,

no

conclusions could be drawn on the _responses attained in each

_direction,

since

pos-sible environmental trends

_and/or

asymmetry

of response could not be

_properly

accounted for in the absence of a control line. General

between-replicate

_agreement

has been found for the

_questions

of interest. In all

_replicates,

a

_{significant divergence}

for the rate of homosexual

_copulation

was obtained

by

practising

direct selection

for this trait. This result

_clearly

shows that the differences between individuals for

the rate of homosexual

_copulation

are

_partly

_genetic

in the

_{Consejo population,}

reinforcing

previous

evidence from diallel

_analysis

of data from

_highly

inbred lines derived from the same

_populations

_(Serrano

et

_al,

_1991).

The

_{evolutionary hypothesis proposed}

_by

Thornhill and Alcock

₍₁₉₈₃₎

assumes

that individuals

_showing

a lower

degree

of sexual discrimination will also have a

higher

sexual

_activity

and may thus achieve

higher

reproductive

fitness. In other

words,

the

_degree

of sexual discrimination

_(represented

_by

the rate of homosexual

copulation)

and sexual

_activity

_(represented

_by

the _average number of

_mountings

for the number of

_mountings

was observed when

selecting

_up and down for the rate

of homosexual

_copulation,

both in each

_replicate

and overall. This

_implies

that the

genetic

correlation between these traits will also be small and not

_significant

in

the

_Consejo

base

_{population, although}

a numerical estimate cannot be calculated from our data. On the other

hand,

the

_{corresponding phenotypic}

correlation was

small but

_significant.

_However,

this

_parameter

contains little information on the

genetic

correlation

and,

in our case, its value is

_compatible

with a zero

_genetic

correlation

_provided

the

_heritability

of the number of

_mountings

is less than 0.95.

Second,

males from the

_upward

selected lines

_(lower

_degree

of sexual

_{discrimination)}

mounted fewer females than those from downward selected lines

_(higher

_degree

of

discrimination)

and, therefore,

the latter are fitter in this

_respect.

The results obtained

by

Serrano et al

₍₁₉₉₁₎

indicate that sex

_recognition

is

absent in T castaneum

_{and, therefore,}

_{homosexuality}

cannot be

_simply

_explained

in terms of

_perception

errors. In the model

proposed by

these

authors,

the

probability

of homosexual

_mountings

_(p

₂

₎

is a function

_only

of the

_composite

_parameter

_a,

which

_represents

the balance between the male’s

_persistence

in

_mounting

and the differential resistance offered

_by

males and females to

_being

mounted. In this

situation,

the behaviour of

mounting

males as well as the differential reactions

of the individuals

_being

mounted

_{(traditionally}

_regarded

as

_passive

partners)

are

taken into account. More

_formally,

_p2 =

1/(1+4a),

where cx =

y/x;

and x and _{y are}

the

_{probabilities}

of homosexual and heterosexual

pair

contacts between individuals

resulting

in

_{mounting respectively. Thus,}

the response to

_divergent

selection can be

analysed

in terms of the

_{corresponding changes}

in the ratio a of these 2

probabilities.

A value

_of

_P2

=

31.6% !

_{1.9 was} estimated

by

Serrano et al

₍₁₉₉₁₎

in the

_Consejo

base

_population.

Our estimate

_{(29.5% !}

_0.74)

does not

_{significantly}

differ from the former

_though

it is

_slightly

lower and

_{significantly}

smaller than

_0.33,

the

expected

value

_{corresponding}

to random

_pair

contacts between

_sexually

indiscriminate

individuals,

when both sexes

being

mounted

equally

_reject.

A _response in the

_upward

direction can be achieved

by lowering

the male’s

general

sexual

_vigour,

in

_{particular by decreasing}

the male’s resistance to

_being

mounted

relative to that of the unselected

_(non-inbred)

females used for

_testing

_(although

not

_necessarily

with _respect to females from the same selected

line).

This does not

need to affect the total number of

_{mountings performed}

_by

a male _{per unit} of

time,

as the

_increasing

difficulties in

_mounting

females may be

compensated by

a

larger

number of homosexual

_mountings.

In

_fact,

the average male’s sexual

activity

was not affected

_by

selection in either direction. In the same

_testing

conditions

of this

_experiment,

_inbreeding

has been shown to enhance the rate of homosexual

copulation by depressing

a male’s

_vigour

(Serrano

et

_al,

_1991).

Therefore,

upward

selection could also act

_through

the same mechanism. In this

_situation,

however,

response to downward selection will be more difficult to

_attain,

as it will

_require

an

increase of the sexual

_vigour

of males above that achieved

_by

natural selection in

the base

_population.

Thus,

the

_asymmetrical

_response found in this

_experiment

is

ACKNOWLEDGMENTS

The authors thank A

_Gallego,

A Garcia-Dorado and B J6dar for

helpful

comments on the

manuscript, and RG Ruano for

laboratory

assistance.

REFERENCES

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₍₁₉₈₂₎

_Dynamics

and genetics of mating behavior in Tribolium casta-neum

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Hill WG

_(1972a)

Estimation of realised heritabilities from selection experiments. I.

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_(1972b)

Estimation of realised heritabilities from selection experiments. II. Se-lection in one direction. Biometrics 28, 767-780

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₍₁₉₇₂₎

Homosexual behavior related to a melanic mutant in Tribolium castaneum.

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_Inf

Bull 15, 97

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₍₁₉₈₉₎

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C

₍₁₉₉₁₎

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₍₁₉₇₁₎

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