Macrogeographic patterns in B-chromosome and inversion polymorphisms of the grasshopper Trimerotropis pallidipennis

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Macrogeographic patterns in B-chromosome and

inversion polymorphisms of the grasshopper

Trimerotropis pallidipennis

Va Confalonieri

To cite this version:

Original

article

Macrogeographic

patterns

in

B-chromosome and inversion

polymorphisms

of the

_grasshopper

Trimerotropis

pallidipennis

VA Confalonieri

Universidad de Buenos

Aires,

Facultad de Ciencias Exactas y

Naturales,

Departamento

de Ciencias

_BioLÓgicas,

Intendente

_Güiraldez

_{y Costanera Norte,}

(1428)

Buenos

_{Aires, Argentina}

(Received

10 June 1994;

accepted

16

February

1995)

Summary - South American

_populations

of

_{Trimerotropis pallidipennis}

are

_polymorphic

for

_pericentric

inversions and B-chromosomes. Previous studies revealed the existence of

_altitudinal,

latitudinal and

_longitudinal

clines for 9 chromosomal sequences, whose

repetition

in

_independent

_groups of

_populations

and over a wide area

_suggested

the

action of natural selection. The

_frequencies

of B-chromosomes were

_analyzed

in 25

_samples

from

_Argentina.

In some of

them,

the B-chromosome interfers with the

_genetic

control of

chiasma

formation,

which is

_partly

conditioned

_by

inversions.

_{Multiple regression analyses}

revealed that the

_frequency

of B-carriers in each

population

is

_{significantly}

associated with latitude

_(negatively)

and

_longitude

_{(positively),}

and that the

frequency

of inversions

significantly

decreases at

_higher

altitudes and latitudes. The _pattern of distribution observed for B-carriers is most

_probably

related to the

_suitability

of habitats. These results

agree with the

parasitic model,

which claims that

_higher

incidence of the B-chromosome

in natural

_populations

is associated with more favorable environments.

Orthoptera

/

polymorphism

/

B-chromosome

_/

natural selection

_/

inversion

Résumé - Répartition macrogéographique des _{polymorphismes} du chromosome B et d’inversion chez la sauterelle Trhnerotropjs pallidipennis. Les

_populations

sud-américaines de

Trimerotropis pallidipennis

sont

_polymorphes

pour des inversions

péri-centriques

et les chromosomes B. Les études antérieures ont révélé l’existence de clines

altitudinaux,

latitudinaux et

_{longitudinaux}

_pour

_{neuf séquences chromosomiques,}

dont les

répétitions

dans des groupes

indépendants

de

populations

et sur une vaste

_{région suggèrent}

l’action de la sélection naturelle. Les

_fréquences

des chromosomes B ont été

_analysées

dans !5

_populations

_{d’Argentine.}

On _peut observer _que dans

_quelques

échantillons le chromosome B intervient dans le contrôle

_génétique

de la

_formation

du

_chiasma,

qui est

conditionné

partiellement

par les inversions. Une

analyse

de

régression multiple

révèle que

inversions diminue

_{significativement en fonction}

de l’altitude et de la latitude. Le modèle de distribution observé pour les porteurs de B est très

_probablement

en relation avec la

qualité

des habitats. Les résultats concordent avec le modèle _parasitaire selon

lequel

de hautes

_fréquences

du chromosome B dans les

_populations

naturelles sont associées à des conditions

_{plus favorables}

de milieu.

orthoptère

/

polymorphisme

/

chromosome B

_/

inversion

_/

sélection naturelle

INTRODUCTION

South American

_populations

of

_{Trimerotropis pallidipennis}

_{(Orthoptera) (2n}

= 23 d

_XO)

are

_particularly

_interesting

from an

evolutionary

_standpoint

because of

the occurrence of

_pericentric

inversions and B-chromosome

_{polymorphisms}

_(Mesa,

1971;

Vaio et

_al,

_1979;

Gobi et

_{al, 1985;}

_{Confalonieri,}

_{1988, 1994;}

Confalonieri and

Colombo,

1989)

contrasting

with North American

_populations

that are

_structurally

monomorphic

(Coleman,

1948; White, 1949,

1951).

Previous studies revealed the existence of

_altitudinal,

latitudinal and

_longitudinal

clines for 9 chromosomal

sequences, whose

repetition

in

_independent

_groups of

_populations

and over a wide

area

_suggested

that natural selection maintains these

_{polymorphisms}

_{(Confalonieri}

and

_Colombo,

_1989;

_{Confalonieri,}

_1994).

Minimum

_temperature

and

_humidity

were

considered as the

_possible

selective

_agents.

With

_respect

to

_genetic

_{recombination,}

inversion

_{polymorphisms}

are also associated to an

_important

chiasma localization

(usually

near or at telomeric

_positions),

which leads to an inverse association between total chiasma

_frequency

and the mean number of

_{heteromorphic}

bivalents

per male

(H)

(Goni

et

_{al, 1985;}

_{Confalonieri,}

_1988).

A B-chromosome was observed

in _{almost every}

_population

from

_Argentina

and in some of them this chromosome is

presumably interfering

with the

_genetic

control of chiasma conditions

_{(Confalonieri,}

1992).

The

_present

_paper

_reports

a

_{macrogeographic}

_pattern

of distribution of

B-frequencies

in relation to those of inversion sequences. These results are

dis-cussed in the

_light

of the

_parasitic

and heterotic models of maintenance of B

poly-morphisms.

MATERIALS AND METHODS

Twenty-five samples

of T

_{pallidipennis}

collected in several

_provinces

of

_Argentina

were

_{cytologically analyzed}

_(table

_I);

159 males

_belonging

to some of these

_samples

were

_previously

studied for chiasma conditions

_{(Confalonieri, 1992).}

Testes were

fixed in 1:3 acetic

_acid/ethanol

and

_squashed

in acetic orcein.

In

_Uspallata,

data

correspond

to the

_sample

of 1991. N:

_sample

size. B: B-chromosome

carrier

_frequency.

H: mean number

_{of heteromorphic}

bivalents _per male. I: mean number of

inverted chromosomes per male. ALT: altitude in meters. LAT and LONG: south latitude and west

_longitude

in

_degrees.

*Data from Confalonieri and Colombo

_(1989).

**Data from Goni et al

_(1985).

RESULTS

Karyotype,

B-chromosome and inversion

_systems

The basic male

karyotype

of T

_{pallidipennis}

consists of 2n = 23 chromosomes which

can be

grouped

into 3 size classes:

large

(L1-L3);

medium

(M4-M8),

including

the

_{X-chromosome;}

and short

_(S9-S11).

The X-chromosome is

_metacentric,

the

large

elements are submetacentric

_(Vaio

et

_al,

₁₉₇₉₎

while both medium and short

chromosomes are

_basically

acrocentric

(Confalonieri, 1988).

The B-chromosome has a distal heterochromatic X-like

_segment

and a

_{proximal isopycnotic region,}

and is a little

larger

in size than the S9 chromosome

(Mesa,

1971;

Vaio et

al, 1979;

Gofii

et

_al,

_{1985; Confalonieri,}

_1988).

In C-banded

_cells,

it shows 2 interstitial

_positively

stained bands which coincide with

part

of the heterochromatic

_region

_(Sanchez

frequencies

of carriers in each

_sample

are indicated in table I. In

_Uspallata,

_stability

of

_B-frequency

was demonstrated in 2 consecutive

_samples

collected in 1991 and

1992 and with

_respect

to a

_sample

of 1984. Six

_pericentric

inversions involve 4 of the medium-sized

_chromosomes,

_producing

_multiple

_karyomorphs

in

_polymorphic

populations

(Vaio

et

_{al, 1979;}

Goni et

al, 1985;

Confalonieri and

_Colombo,

_1989).

Macrogeographic

patterns

In order to assess

_possible

_patterns

of distribution of

_{B-frequencies,}

data from 20

samples

collected in a wide altitudinal

_(ALT),

latitudinal

_(LAT)

and

_longitudinal

(LONG)

range were used in addition to 5

_samples

from south

_Argentina

_reported

in Goni et al

_(1985).

Table I shows the

_frequencies

of B-carriers in each

_sample,

together

with the mean number of

_{heteromorphic}

bivalents

_(H)

and inversions

(I)

per male per

population.

Results of

_multiple

_regression

of these 3

dependent

variables on

_ALT,

LONG and LAT are

presented

in table II. Two distinct

_patterns

of variation were observed for 2 kinds of

_{polymorphisms.}

The first clear

_pattern

is

demonstrated _{for supernumerary} chromosomes so that the

_frequency

of B-carriers in each

sample

is

_{significantly}

associated with its latitudinal and

_longitudinal

situation.

Secondly,

the

_frequency

of inversions is

_highly

associated with latitude and altitude in such a _{way that inversions tend} to

_disappear

at

_higher

latitudes and altitudes. As

_previously

shown

_{(Confalonieri}

and

_Colombo,

_1992),

both clines indeed reflect a minimum

_temperature

_dependence.

The level of inversion

_polymorphism

(measured

through

the

_parameter

_H)

did not show a clear

_{macrogeographic}

pattern

of variation because maximal values are attained at intermediate altitudes and

latitudes,

so the clines observed

_depend

on which _groups of

_populations

are scored. T

_{pallidipennis,}

which is endemic to North

_America,

is 1 of the few

trimero-tropines

to have

_successfully

extended its distribution to Andean South America

(Vaio

et

_al,

_1979),

_being

_adapted

here to a wide altitudinal range. Rain forests and

humid_grasslands

(in

eastern

_localities)

are not inhabited

_by

this

_species

and its basic

requirement

appears to be the

prevalence

of arid and semi-arid conditions.

(table

I)

correspond

to

populations

considered

by

these authors as

marginal,

because

they

are situated at the southern border of the

_species

_range.

_Therefore,

more

eastern

_longitudes

and southern latitudes are most

_probably

_marginal

environments for T

_{pallidipennis,}

_just

where the

_frequency

of B-carriers tends to be lower.

DISCUSSION

The

_longstanding

debate about B-chromosomes revolves around the issue of whether these

_{widespread polymorphisms}

are

_simply

a direct result of the

accu-mulation mechanisms or whether

_they

derive from the action of natural selection

(Jones, 1985).

The view

_presently

favored inclines to the so-called

_{’parasitic’}

model

which _argues that B-chromosomes are selfish elements and drive is the main force

generating

this kind of

_polymorphism

_(Jones,

1991;

Shaw and

Hewitt,

1991).

An

extreme case of selfishness has been

_recently

_reported

_by

Nur et al

_(1988).

However,

a

_great

_variety

of mechanisms of

_{drive, phenotypic}

effects and

_origins

have been described for B-carriers

_belonging

to different

_species

and even to

populations

of the same

_species

(Jones

and

_{Rees, 1982; Jones, 1985, 1991;}

Bell and

Burt,

1990;

Shaw and

_{Hewitt, 1991;}

_Bougourd,

_1993).

It thus seems

_{inappropriate}

to

_{unequivocally}

ascribe a universal model of maintenance for all B-chromosome

polymorphisms.

The 2 distinct

_patterns

of variation observed for both B-chromosomes and

structural

_{rearrangements}

in T

_{pallidipennis correspond}

to different processes of

evolution.

All inverted _sequences tend to increase in

_frequency

towards lower altitudes and

latitudes. These clines

_{probably respond}

to

_{geographically}

_varying

selection related

to some climatic variables

(Confalonieri, 1994).

Moreover,

some

_enzymatic

loci could

be in

_linkage

_{disequilibrium}

_{with supergenes maintained}

_by

_inversions,

which

_might

be the

target

of selection.

The clines observed _{for supernumerary chromosomes}

following

geographical

variables are better

_{explained by}

means of the

_parasitic

model: B-carriers are

obviously

most

_frequent

in those areas where the

species

thrive and

disappear

in circumstances where the burden on fitness is too

_heavy

to

_bear,

ie in

_marginal

environments. Similar situations were found in

_{Mymneleotettiz}

_maculatus,

where

B-carriers are limited to

_populations

in the south and east of Great Britain which

are

_climatically

better for

_grasshoppers

(Hewit

and

_{Brown, 1970; Hewitt,}

1973),

and in

_{Crepis capillaris,}

where

_{higher B-frequencies}

are also the reflection of the

suitability

of the habitats

_(Parker

et

al,

1991).

Some of the

_phenotypic

effects of B-chromosomes concerned with recombination at meiosis have often been considered to be of

adaptive importance

(Jones

and

_Rees,

1982).

However,

this view has

_recently

been reconsidered

_(Bell

and

_{Burt, 1990;}

Shaw and

_Hewitt,

_1991).

Bell and Burt

₍₁₉₉₀₎

_proposed

the

_theory

of ’inducible

recombination’

_by

which individuals with

_{’parasitic’}

B-carriers

_might

be

_expected

to

increase recombination

_amongst

the autosomes so that new

_genetic

variants that are

resistant to infection

by

B-carriers would be more

_likely

to arise. In

_fact,

the presence

of B-carriers is

_usually

associated with an increase in chiasma formation

(Jones

and

Rees, 1985;

Bell and

Burt,

1990).

On this

_theory,

successful

_{’B-parasites’}

would be

significant

decrease of mean chiasma

_frequency

of B-carriers was verified for some

populations

(Confalonieri,

1992).

This effect of B-chromosomes could then be of

significance

to the

_long-term

survival and evolution of local

_populations,

_especially

those in less favorable environments.

ACKNOWLEDGMENTS

I wish to express my sincere thanks to JH Hunziker for critical

reading

of the

manuscript.

Financial _support from the

_Consejo

Nacional de

_{Investigaciones}

Cientificas y T6cnicas and

Universidad de Buenos

_{Aires, through}

_grants to JH Hunziker and JC Vilardi.

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