Seasonal fluctuations of cosmopolitan inversion frequencies in a natural population of Drosophila melanogaster

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Seasonal fluctuations of cosmopolitan inversion

frequencies in a natural population of Drosophila

melanogaster

F Sanchez-Refusta, E Santiago, J Rubio

To cite this version:

Original

article

Seasonal

fluctuations

of

_cosmopolitan

inversion

_frequencies

in

a

natural

population

of

_Drosophila

_melanogaster

F

Sanchez-Refusta*

E

_Santiago

J Rubio

Universidad de _{Oviedo, Departamento} de _Biologia Funcional

_(Genética),

33071 _{Oviedo, Spain}

(Received

10 June _{1988; accepted} 30 October

₁₉₈₉₎

Summary - Seasonal

_changes

in the frequencies of _cosmopolitan inversions and

_In(3R)C

have been

_investigated

in a _{Spanish population} of _{Drosophila melnnogaster for 4 years.}

Regression and Fourier analysis methods were used to separate the _temporal variation of the _frequencies into linear and _cyclic components. Different _patterns in _temporal variation

were detected. The _frequency of

_In(2R)NS

was _stable;

_In(3R)C

tended to increase its

frequency

across _{the years;}

_In(3R)P

showed oscillations that could not be attributed to

_{cyclic changes.}

_In(2L)t

and

_In(3L)P

showed seasonal

_{cyclic changes}

with

_increasing

frequencies during

the warm months, which are

_thought

to be

_mainly

due to the _superior relative fitness of _{heterozygotes,} as _compared with inversion non-carrier individuals. The

fall of _frequencies in the cold months is

_probably

a consequence of the shorter life-span of the carriers of these inversions

_during

the winter. The differences between the

temporal variation _patterns of the inversions do not _support the _hypothesis of a

_single

climatic factor as

_being

_responsible for the _geographic cline of the

_cosmopolitan

inversions. Without

_ignoring

the influence of

_underlying

selective factors of macroclimatic nature, other

_ecological

and

_genetical

factors uncorrelated with latitude are

_suggested

to _play a

role in the _temporal

_dynamics

of the _inversions, as well as in their

_geographic

distribution.

Drosophila melanogaster / inversion _{frequency /} seasonal change

Résumé - Fluctuations saisonnières des fréquences d’inversions _cosmopolites dans

une _population naturelle de _{Drosophila melanogaster -} Les variations saisonnières des

_fréquences

de

_plusieurs

inversions

_cosmopolites

et de

_In(3R)C

ont été étudiées dans

une _population

_espagnole

de _Drosophila

_{melanogaster pendant}

_{¢ ans.} Des méthodes de

régression

et

_d’analyse

de Fourier ont été utilisées _{pour séparer} les variations

_temporelles

en _composantes linéaires et en _composantes

cycliques.

On a détecté

différents pm

f

i

l

s

de

variation _temporelle. La _fréquence de l’inversion

_In(2R)NS

est restée stable, celle de

In(3R)C

a eu tendance à croître au cours des années, celle de

_In(3R)P

a montré des

oscillations non périodiques. Les fréquences de

In(2L)t

et de

_In(3L)P

ont montré des variations saisonnières _cycliques, avec un accroissements des

fréquences

pendant les mois

chauds,

qu’on peut rattacher à une

_fitness

relative

_supérieure

des

_{hétémzygotzes}

par rapport

aux individus non _porteurs d’une inversion; la baisse des fréquences pendant les mois

froids est _probablement une _{conséquences} de la durée de vie _plus brève des _porteurs de ces

*

inversions pendant les mois d’hiver. Les _différences de _profils des variations saisonnières de ces inversions ne _{sont pas} en accord avec _{l’hypothèse} selon _laquelle un seul

_facteur

climatique serait responsable du _{gradient géographique} des _fréquences des inversions

cosmopolites. Sans exclure _{l’influence} de _facteurs

_sélectifs

_{d’origine microclimatique,} on

suggère que d’autres facteurs écologiques et _{génétiques,} non corrélés avec la latitude,

joueraient un rôle dans la dynamique temporelle des fréquences des inversions ainsi que

dans leur _{répartition géographique.}

Drosophila melanogaster / fréquence d’inversion _/ variation saisonnière

INTRODUCTION

Natural

_populations

of

_{Drosophila melanogaster}

are

_polymorphic

for chromosome

inversions;

especially

for the 4 inversions termed &dquo;common

_{cosmopolitan&dquo; by}

Mettler et al

_(1977).

These are:

In(2L)t, In(2R)NS,

_In(3L)P

and

_In(3R)P.

_Strong

latitudinal clines in the

_frequencies

of the 4 inversions have been described in the

USA

_(Mettler

et

_al,

_1977;

_Stalker,

_1980),

_Japan

_(Inoue

and

_{Watanabe, 1979;}

Inoue et

_al,

₁₉₈₄₎

and Australia

_(Knibb

et

_{al, 1981;}

Anderson et

_al,

_1987).

The

_frequency

of each inversion diminishes the further it is from the equator. This seems to be

a

_{general feature, despite}

the results found in

_Japanese

_{populations by}

Inoue et al

(1984),

where the lack of correlation between latitude and

_frequency

of

_cosmopolitan

inversions could be due to the small scale of

_sampling

_(Anderson

et

_al,

_1987).

The

_parallel

chromosomal

_changes

with latitude _suggest an

adaptation

to

eco-logical

differences associated with climate

_{(explanations}

_{involving only}

random pro-cesses can be discounted

_by

the similar directions in the two

_{hemispheres).}

Eco-logical

differences are

obviously

diverse and

complex.

In a revision

work,

Knibb

(1982)

studied the _{correlation among the}

_frequency

of inversions and some

macro-climatic variables. He found that the

_frequencies

were

_generally

_positively

correlated

with _temperature. Stalker

₍₁₉₈₀₎

found

_{temperature-dependent}

differences between

karyotypes

in

_flying

_ability.

But no causal effect of _temperature on inversion

fre-quencies

may be asserted. At present, the cause of the latitudinal cline is an _open

problem.

If the reason were

_simply

the

_adaptation

of inversion carrier individuals to

_higher

temperature, some

_periodic

seasonal fluctuations of the inversion

_frequency

should

be detected. In

_fact,

Stalker

₍₁₉₈₀₎

found a

_significant

shift from

_May

to October of the inversions on the

_right

arms of chromosomes II and III. Knibb

(1986)

_reported

seasonal variations

_repeated

over _{2 years} for

In(2R)NS

and

_In(3L)P.

Two other

works deal with seasonal fluctuations

_{(Zacharopoulou}

and

_Pelecanos,

_1980;

Inoue et

_al,

_1984),

but no

significant

_{periodical changes}

were detected.

In this _paper, we describe a

temporal

evolution of the chromosomal

polymor-phism

in a Northern

Spanish population

in

Drosophila melanogaster

for 4 years. We _present evidence that

_periodical

seasonal

_{changes play}

an

_important

role in the

dynamic

of inversion

_frequencies

of this

_population,

but there are clear differences

between

_temporal

data and that

_expected

from 1

_single

selective climatic factor

MATERIALS AND METHODS

Wild flies were

_captured

in a

_nearby

wood

_(Los

_Areneros;

7 km from

_Oviedo;

43.2°

latitude,

5.9°

_longitude).

_{Twenty-one samples}

were collected around the 15th

day

of each month from June to November in the years 1981-1984

(samples

were taken in

_July

_1981,

_August

1982 and

_August

_1984).

Banana and

_live-yeast

traps were left

in the wild for 3

_days;

flies were collected in the afternoon.

Females inseminated in nature were

kept individually

in

vials,

and

salivary

gland

chromosomes from a

_single

larva of the progeny of each vial were examined.

Chromosomes were

_prepared

as described

_by

Levine and Schwartz

(1970).

Because of data type and the different

_sample

_sizes,

the

_temporal

trend

_analyses

were

_performed

_{by using}

the least

_X

₂

method.

_First,

temporal

inversion

_frequencies

were

analysed

to detect linear trends. The

_{monthly frequencies}

were

adjusted

to a linear

_regression

on the ordinal number of each month

(from

1 to 48 across the 4 _years,

_although

a few months are

_missing).

The

_X

₂

_ldf

value to test the linear trend

_hypothesis

was calculated as the difference between the

_{heterogeneity}

among

samples

_X2odf

and the

_adjusted

linear

_regression

deviation

_{X19df- 2}

Secondly,

statistical

_analysis,

in order to detect a

_{year-by-year cyclic}

variation

pattern, was

performed.

Fourier series

_equations

with

_only

1

_harmonic,

frequently

used in

_analysis

of

_sequential

data

_(Yule

and

_Kendall,

_1950),

were

_applied.

As linear

trends were

_detected,

the Fourier

_equations

were corrected for the linear trend. The

general

periodic equation

which expresses the

expected

inversion

frequencies

(Yi)

for every month

(x

i

)

can be written as:

with C = cos

₍₂

₇

_nr,)/0;

S = sin

(2

7

r

Xi

)/()

where B is the

period

in

_months;

_¡.t, a

(regression coefficient),

and a

and (3

are the

coefficients of the modified

_{periodic equation.}

The x variable can take any value

between 1 and 48. If inversion

_frequencies

were

_really

_fluctuating

_according

to a

yearly cyclic

pattern, the

_adjustment

to the

_periodic

equation

would be better for

a

_period

of around 12 months. If this is not so, the

previous

adjustment

is

_thought

not to be

_significant

and does not

_improve

other 0 values.

_{Consequently,}

for each inversion

_{frequency series,}

11

_equations

were

performed corresponding

to the 11

values of 0

_ranging

between 7 and 17 months. The

_{X 2}

_d

_{f 2}

value to test the

_cyclic

pattern

hypothesis

for each 0

value,

is estimated as the difference between the linear

regression

deviation

_X

_î

_9df

_previously

_calculated,

and the

_{corresponding periodic}

equation

deviation

_X

_î

_7df

_(p,

a, a

and /3

are estimated in this

_adjustment).

To allow

_comparisons

_among different

_{period adjustment}

_equations,

the 11

_X

_i

_df

values for each inversion are

_{plotted against}

the

_{corresponding}

0 values on a

_{&dquo;periodicity}

testing&dquo;

chart. All the least

_X

₂

_adjustments

were made

_{by using computer-aided}

approximations.

Average monthly

temperature

and rainfall were used to check the correlation of macroclimatic data with the inversion

_frequencies.

The correlation coefficients of

Spearman

(rs

lsdf

)

were calculated between the serial

_frequencies

of each inversion

and the 2 macroclimatic variables for the

_trapping

month,

as well as for the

previous

7 months. Climatic data were obtained from the Observatorio

Meteorol6gico

de

RESULTS

The most abundant

_Drosophila

_genus

_species

found

_during

the

_{trapping period}

were D

_{melanogaster,}

D

_immigrans

and D simulans. D

_melanogaster

was dominant in

June and

_July,

but D simulans increased

_{rapidly, becoming}

most abundant

_during

August

and

_September.

The number of individuals

_caught

in November decreased

drastically, becoming

null from December to

_May.

Many

inversions were

_found,

some of them described for the first time

_(Roca

et

al,

1982).

However,

in this work we shall deal

only

with those that were

sampled

at a

frequency

over 5%. These were the 4 common

cosmopolitan

inversions and the

In(3R)C,

labelled as &dquo;rare

cosmopolitan&dquo;

_by

Mettler et al

_(1977).

The

_frequencies

of

these

_polymorphic

inversions in the various

_{samples during}

the _years 1981-1984 are

given

in Table 1.

_Only

_In(2R)NS

did not _present

_{significant changes}

in

_frequency;

nevertheless,

linear trend

_X2

_ldf

was

_significant,

_although

_{very close} to the 0.05 limit.

The 2 inversions on the

_right

arm of chromosome III showed an

_increasing

_frequency

trend with time. This trend was

_{highly significant}

for

In(3R)C,

which increased

at a rate of 2.2% each _year. In

_fact,

the linear

_{regression explains}

most of the

temporal

frequency changes

of this inversion: the

_remaining

_XI9d!’

after the linear

regression adjustment,

was

_significant

_only

at the 0.05 level.

_Fig

1

_graphically

shows

The

_{&dquo;periodicity testing&dquo;}

charts

_{(Fig 2)}

_clearly

underline the differences _among the inversions. As

_{expected, periodic}

fluctuations were not detected either for

In(2R)NS (where

sampling frequencies

were

_{homogeneous),}

or for

_In(3R)C

_(where

the linear trend

_explains

most of the differences _among

_{samples). In(2L)t}

showed a

maximal

_{significant adjustment}

for the 12-month

period.

The

_remaining

deviations

after the

_adjustment

to the 12-month

_periodic

_equation

were not

_significant

_(x

_i

_7df

=

23.5).

This

_implies

that the

_fluctuating

pattern of this inversion is

_{mainly periodic;}

being repeated

every year.

In(3L)P

also showed a maximal

adjustment

to a 12-month

_period.

However,

two observations should be noted:

_first,

there was 1

_peak

for the 9-month

_{period length,}

and

_second,

all the

_adjustments

to different

_period

equations

were

_significant.

The wide

_wandering

fluctuations

_{of In(3L)P}

_frequencies,

together

with the lack of

_samples

for some

months,

allowed a _great

_variety

of

periodic

series to fit the data. In _{any case,} the

_finding

of a

_{figure shape,}

with a maximum for a

nearby

12-month

period,

indicates the existence of a _year-to-year

periodic

pattern. The

_remaining

_In(3L)P

_deviations,

after

_adjustment

to the

12-month

_{period function,}

were

_{highly significant}

(

X

’

17df

=

_40.9;

P _<

0.001).

_Finally,

the

_analysis

of

_In(3R)P

evolution sheds no

_light

on the existence of the

cyclic

component: the

_X2df

value for a 12-month

_period

is not the

_maximum,

_{being only}

significant

at a level _very close to 0.05.

The

_cyclic

pattern of

_In(2L)t

and

_In(3L)P

_frequency

fluctuations is

_strong

evidence that a selective process is

taking place

(Lewontin, 1974),

and that the

relative fitness must be

_changing

over the _year. It is

_possible

to estimate the confidence limits within which the relative fitness in a

_given

season would lie

when

_changes

occur

_rapidly

and

_repeatedly,

as done

_{by Dobzhansky}

₍₁₉₄₃₎

for D

_{pseudoobscura}

third chromosome inversions. Both inversions increased their

frequency during

the

_{period ranging}

from June to

_September,

when the mean

temperature was around 18°C. At this _temperature, the

_development

time is close

to 16

_days

_(David

and

_Clavel,

_1967).

_According

to the _egg

_laying

curves

_computed

by

McMillan et

_{al (1970) (laboratory}

conditions at

_{25°C), the}

mean _egg

_laying

could be around 9 d.

So,

the mean

_generation

time could be near 25 d.

Obviously,

the

effect of microclimate deviations and other

_ecological

factors cannot be evaluated.

It is reasonable to assume that the

_generation

time would lie between 20 and 30 d.

Because of the low

_frequency

of these 2 inversions over the 4 months

_(In(2L)t

had a mean

_frequency

of 22% and

In(3L)P

of

18%),

there is

_likely

to be a low

_frequency

of inversion

_homozygotes,

so that the

_biological

fitness of the inversion

_homozygote

of each inversion should

_mainly

be a result of

_greater

heterozygote

fitness in relation to the

_homozygous

standard _arrangement. As the

_In(2L)t

_frequency

increase was

3.37% per

month,

the relative fitness of the

heterozygote

should lie between 1.18 and 1.28

_(for

20 and 30 d of

_generation

time,

respectively). In(3L)P

showed a

_frequency

mean increase of 2.71% _per

_month,

so the relative

_heterozygote

fitness should be

between 1.16 and 1.25.

Knibb

₍₁₉₈₆₎

found a

_positive

and

significant

correlation of inversions

In(2L)t,

In(2R)NS

and

_In(3L)P

with the _temperature and rainfall of the

previous

month. Our data reveal that the

_In(2L)t

frequency

was

positively

and

significantly

corre-lated with the mean _temperatures in the 2nd to 5th months

_previous

to the

trap-ping;

the correlation was maximized with the temperature of the 3rd

_previous

month

(rs

=

_0.54,

P _<

0.01).

The

frequency

of In(2L)t

_was also

negatively

correlated with

rainfall in the 3rd and 4th months

_previous

to the

_trapping.

In this _case, the cor-relation was maximized in the 3rd month

(rs

=

_0.66,

P _<

0.01). In(3L)P

showed _a

positive

and

_significant

correlation with the mean temperature of the month

previ-ous to the

_trapping

_(rs

=

0.38,

P <

_0.05),

and was

_negatively

correlated the rainfall in the

_previous

2

_months,

_especially

in the first one

_(rs

=

-0.52,

P <

_0.01).

The

remaining

2 inversions showed a

significant

correlation with the mean _temperature of 2 months:

_In(3R)P

with the 2nd

_previous

month

_(rs

=

0.49,

P _<

0.05)

and

In(3R)C

with that of the

_trapping

month

_{(rs =}

_0.40,

P <

_{0.05). In(3R)P}

also

showed

_significant

correlations with rainfall of the 6th

_(rs

=

_-0.41,

P _<

0.05)

and

7th

_(rs

=

_-0.41,

P _<

0.05)

_previous

months.

Because of the _great number of tests

_performed,

these correlation coefficients

must be

_interpreted

with care

(especially

the p > 0.01

_{significant ones).}

_So,

only

In(2L)t

and

_In(3L)P

are reliable

_enough

to be considered. But we cannot presume a causal effect of temperature and rainfall on the

_cyclic

_pattern of inversion

frequencies

as there are many other environmental variables which follow a

_cyclic

pattern and could be correlated as well.

Conversely,

a causal effect cannot be ruled out. The fact that the

_frequency

of

_In(2L)t

had a maximal correlation with the _temperature and rainfall of the

3rd

previous

month could be the result of climatic selection

_acting

on the whole

population,

and that would not reach

_{equilibrium instantaneously. Notably,}

there

was a _very

_interesting

fact

_supporting

the climatic cause in

_{frequency changes}

that

may be mentioned: the 1981-82 winter mean _temperature was

remarkably

warm

(near 10°C) (Fig 1).

In

_1982,

_In(3L)P

reached its

_highest

_frequencies

within those 4 years; that year,

jointly

with

1984,

In(2L)t

reached its

highest frequencies

as well.

DISCUSSION

The

_geographic

distribution of 4

_cosmopolitan

inversions of D

_melanogaster

(Mettler

et

_al,

_1977;

Inoue and

_Watanabe,

_1979;

_Stalker,

_1980;

Knibb et

al, 1981;

Inoue et

_al,

₁₉₈₄₎

_suggests

that common selective factors are

_operating.

The ex-istence of a latitudinal correlation in both

hemisphere

_suggests that the selective

factors are related to some climatic variable. In

fact,

Knibb

(1982)

found the

If _temperature were the direct selective factor

_responsible

for the latitudinal

cline,

a

_joint

oscillation of the 4 inversion

frequencies

would be

expected,

with a maximum

_occurring

in the warmest months. Our

_results,

however,

do not support

this

_supposition.

In

_fact,

we have found several _patterns:

In(2L)t

and

In(3L)P

underwent

_{cyclic frequency changes;}

_In(2R)NS

remained stable

_throughout

the 4 years;

In(3R)P

showed no

cyclic

oscillations,

while

In(3R)C

tended to increase its

frequency

with the years.

The

_cyclic

behavior of

_In(2L)t

and

_In(3L)P

is _strong evidence that

_they

are sub-mitted to seasonal selective factors. The increase in their

_frequencies

in the hottest months agrees with

geographic

distribution correlated with _temperature, and a di-rect selective effect of temperature is

_certainly

a _very

tempting hypothesis.

The

cycle

of

_frequencies

of these inversions can be

_{explained by heterogeneous}

environ-ment over

_time,

as follows:

_during

the hot months the

frequency

increases due to the selective

_advantage

of

_heterozygous

individuals. There are 2

_previous

observations on

_In(2L)t

that are in accordance with this.

_First,

there is a

_higher

productiv-ity

of

_In(2L)t

_{heterokaryotypic}

females in

_population

_cages at

_high

_temperatures

(Watanabe

and

_{Watanabe, 1973;}

_they

refer to

_In(2L)t

as

In(2L)B).

Second,

there is a

_positive

correlation between _temperature and

flying

activity

in those individuals

carrying

inversions

_especially

on the left arm of chromosome II

(Stalker, 1980).

In

the winter

_time,

D

_{melanogaster populations}

survive as adult flies that can

with-stand,

for

_nearly

200

_days,

_temperatures close to 10°C

_(Lumme

and

Lakovaara,

1983;

David et

al,

1983).

As

Drosophila development

is

_{only possible}

between 12°C

and 32°C

_(David

et

_al,

_1983),

and

_considering

that the mean _temperatures from December to

_{April hardly}

ever goes over

12°C,

there will be _very few

_generations

during

the months of

_{non-trapping.}

The fall of

_In(2L)t

and

_In(3L)P

_frequencies

would

_probably

be a consequence of a weaker resistance to cold or to a shorter

life-span

of the carriers of these inversions.

In any case, the

cyclic

fluctuations

reported

in this work cannot be

generalized.

Stalker

₍₁₉₈₀₎

_reported

a

significant

increase in the

frequency

of inversions from

spring

to

_fall,

but

_only

on the

_right

arm of chromosomes II and III. Knibb

(1986)

found seasonal

_{cyclic changes}

in the

_frequencies

of

_In(2R)NS

and

_In(3L)P

over the 2 years he studied.

Despite

the different

results,

those inversions that underwent

year-by-year cycles

reached a maximum

frequency

in the warmest months.

The overview of

_geographic

distribution data

_points

towards an

_origin

due to

macroclimatic factors associated with

_{latitude, although,}

as

pointed

out

_by

Knibb

(1986),

a free inversion effect in

marginal populations

could also be

implicated

(Lewontin, 1974).

On the other

hand,

the different

_temporal

variation _patterns in

different areas indicate that other factors are

working.

First,

the

ecological

differ-ences _among localities will condition the

_adaptative

response of the

populations

according

to seasonal environmental

_{changes (inversion}

could be

_implicated

in this

response).

Inoue et al

₍₁₉₈₄₎

noted the

_importance

of non-climatic environmental

changes

for latitudinal cline deviations.

_Second,

the

_genetic

differences for the same inversion among different

_{places, resulting}

from selective or random _processes, could

certainly

contribute to a differentiation of the response to environmental

_changes.

Evidence of

_genetic

differentiations in this sense was obtained

_by

Voelker et al

are not

_completely

_explained

_by

the clines of those inversions.

By

including

this

fac-tor, we are also in _agreement with Fontdevilla et

al,

(1983),

who

_suggested

that the chromosome _arrangement be considered as a set of _{supergenes which} could

_respond

in different ways,

depending

upon the environment.

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