The subfamily Lygaeinae comprises 58 genera with about 500 species distributed world-wide. Despite the great biodiversity of the taxon, cytogenetic data of the group is scarce. To date, only 26 species belonging to 12 genera have been cytogenetically described. As it is the rule for the order Heteroptera, all the species possess holokinetic chromosomes, and a pre-reductional type of meiosis, namely at anaphase I the autosomal bivalents divide reductionally while the sex chromosomes are achiasmatic and divide equationally. Available data reveal that all the Lygaeinae are characterised by a modal diploid number of 14 and an XY/XX sex chromosome determining system. In the present study the male meiotic development of Lygaeus alboornatus from Argentina is analysed. The results demonstrate that the species, though sharing the basic chromosomal features from Lygaeinae, has a diploid number of 12 (10+XY), being this chromosome number the lowest reported so far for the subfamily.Facultad de Ciencias Naturales y Muse

Bressa, María José

Larramendy, Marcelo Luis

Papeschi, Alba G.

Caryologia

English

SEDICI - Repositorio de la UNLP

CARYOLOGIA Vol. 55, no. 1: 15-19,2002
Meiotic studies in Lygaeus alboornatus Blanchard 
1852 (Heteroptera, Lygaeidae, Lygaeinae)
María José Bressa1, Alba G. Papeschi2 and Marcelo L. Larramendy1' *
* Corresponding author: fax ++54 221 423 3340; e-mail: 
m_larramendy@hotmail.com
1 Laboratorio de Citogenètica y Cátedra de Citología, Facultad de Ciencias Naturales y Museo, Universidad Nacional de 
La Plata, Calle 37 Nro. 668 7mo “B", 1900 La Plata, Argentina.
2 Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, 
Argentina.
Abstract - The subfamily Lygaeinae comprises 58 genera with about 500 species 
distributed world-wide. Despite the great biodiversity of the taxon, cytogenetic 
data of the group is scarce. To date, only 26 species belonging to 12 genera have 
been cytogenetically described. As it is the rule for the order Heteroptera, all the 
species possess holokinetic chromosomes, and a pre-reductional type of meiosis, 
namely at anaphase I the autosomal bivalents divide reductionally while the sex 
chromosomes are achiasmatic and divide equationally. Available data reveal that 
all the Lygaeinae are characterised by a modal diploid number of 14 and an 
XY/XX sex chromosome determining system. In the present study the male mei­
otic development of Lygaeus alboornatus from Argentina is analysed. The results 
demonstrate that the species, though sharing the basic chromosomal features 
from Lygaeinae, has a diploid number of 12 (10+XY), being this chromosome 
number the lowest reported so far for the subfamily.
Key words: Heteroptera, Lygaeinae, Lygaeus alboornatus, Meiosis, Holokinetic 
chromosomes.
INTRODUCTION
Members of the large and diverse family Ly­
gaeidae are so-called seed bugs. Though the 
taxon was first recognised as a higher group by 
SCHILLING (1829) and the first and most com­
plete early synthesis was performed by STAL 
(1872), it was not until 1964 when SLATER 
(1964) provided a modern world catalogue. The 
Lygaeidae are probably paraphyletic, with some 
of the subfamilies being the sister taxa of mem­
bers of other insect groups namely Bertydae, 
Colobathristidaae and Malcidae (SOUTHWOOD 
and LESTON 1959; STYS 1967). Consequently, 
the family is taxonomically difficult to charac­
terise, and the complex relationships among its 
members are far to be determined (SCHUH and 
SLATER 1995). So far, 16 subfamilies comprising 
at least 500 genera and approximately 4000 
valid species are distributed in all faunal regions 
both in the Old and in the New Worlds (SCHUH 
and SLATER 1995). Within Lygaeidae, the sub­
family Lygaeinae represents a large taxon found 
world-wide with fifty-eight genera with about 
500 species currently recognised. As with most 
lygaeid taxa, the greatest diversity is found in 
the tropical and subtropical regions (SCHUH 
and Slater 1995).
Despite the wide biodiversity of the Ly­
gaeinae, only 26 species belonging to 12 genera 
have been cytogenetically analysed so far 
(UESHIMA and ASHLOCK 1980). As it is charac­
teristic of Heteroptera, all the species possess 
holokinetic chromosomes and a pre-reduc- 
tional type of meiosis: at first meiotic division 
the autosomal bivalents divide reductionally 
while the sex chromosomes are achiasmatic 
and divide equationally. Available data confirm 
that all species are characterised by the lack of 
a pair of m chromosomes; they have an XY/XX 
(male/female) sex chromosome determining 
16 BRESSA, PAPESCHI and LARRAMENDY
system, and a modal diploid number of 14 
(UESHIMA 1979). Moreover, only three species 
are cytogenetically exceptional by having a 
higher chromosome number, most probably 
due to fragmentation of either autosomes or the 
X chromosome (Ueshima 1979): Lygaeus simu- 
lus (Parshad 1957) and Oncopeltus famelicus 
(UESHIMA 1979) possess 2n= 22 (20+XY) chro­
mosomes, while a diploid chromosome number 
of 15 (12+X1X2Y) has been reported for Aro- 
catus suboeneus (Ueshima 1979). The latter is 
the only species of the subfamily with a multi­
ple sex chromosome determining system.
In the present study the male karyotype and 
meiotic development of Lygaeus alboornatus 
from Tornquist Park (Buenos Aires Province, 
Argentina) is described and discussed.
MATERIAL AND METHODS
Specimens and locality
The material included in the present study com­
prises 12 adult males of Lygaeus alboornatus collected 
in November 1996 and in December 2000 in Torn­
quist Park (Buenos Aires Province, Argentina). Three 
specimens were not included in the meiotic analysis 
since only spermatids were found in testes (Specimens 
10-12, See Table 1).
Cytogenetic analysis
Immediately after capturing, all specimens were 
fixed in methanokglacial acetic acid (3:1), and main­
tained at 4°C until dissection. Afterwards, gonads 
were dissected free and kept in ethanol 70% (4°C). 
Slides were made by the squash technique in 2% iron 
acetic haematoxylin following conventional proce­
dures.
RESULTS
Lygaeus alboornatus possess a male diploid 
chromosome number of 12 (10+XY). An auto­
somal pair is easily identified due to its large size 
among the remaining four pairs of autosomes. 
The sex chromosome determining system is 
XY/XX, being the Y chromosome the smallest 
element of the complement (Fig. 1A). At zy­
gotene the sex chromosomes X and Y are posi­
tively heteropycnotic and lie close to each other, 
but they are usually separated at pachytene 
(Fig. IB). During the diffuse stage the autosomal 
bivalents decondense completely while the sex 
chromosomes continue positively heteropycnotic 
and lie either separated or close to each other 
(Fig. 1C). At diplotene-diakinesis the X and Y be­
come isopycnotic and are always separated (Fig. 
1D-F). At late diakinesis the Y chromosome be­
comes negatively heteropycnotic. At metaphase I, 
both the X and Y univalents orientate side-by- 
side at the centre of the ring formed by the five 
autosomal bivalents (Fig. 1G). At anaphase I, the 
autosomal bivalents divide reductionally while 
the sex chromosomes segregate equationally. 
Second metaphase follows immediately after 
telophase I without an intervening interkinesis 
stage. At metaphase II, the autosomes dispose 
again forming a ring while the X and Y chromo­
somes come close together and associate to form 
a pseudobivalent, which lies at the centre of the 
ring (Fig. 1H). At anaphase II, the X and Y seg­
regate to opposite poles.
Autosomal bivalents present at least one ter­
minal chiasma, although the largest bivalent, and 
less frequently other bivalents, can show two chi- 
asmata (Fig. 1G). Cells with two ring bivalents
Table 1 - Mean chiasma frequency and percentage of cells with univalents at diakinesis-metaphase I in the specimens of 
Lygaeus alboornatus from Tornquist Park (Buenos Aires Province, Argentina).
Individual Code Number 
of cells
Mean 
chiasma 
frequency
% of cells 
with 
univalents
1 210696 5 6.20 nd
2 220696 35 6.00 14.29
3 230696 42 5.30 9.52
4 990473 20 5.70 5.00
5 990474 23 5.78 0.00
6 990475 64 5.62 9.37
7 990476 46 5.63 15.22
8 990477 46 5.60 6.52
9 990478 25 5.96 0.00
nd, frequency of cells with univalents not determined due to the reduced number of cells analysed.
MEIOTIC CHROMOSOME BEHAVIOUR OF LYGAEUS ALBOORNATUS 17
Fig. 1 - Lygaeus alboornatus Blanchard 1852. (A) Mitotic prometaphase; (B) Pachytene; (C) Dif­
fuse stage; (D) Diplotene; (E) Diakinesis with the largest bivalent with one interstitial chiasma; 
(F) Diakinesis with the largest bivalent with a terminal chiasma; (G) Metaphase I with the largest 
bivalent with two chiasmata; (H) Metaphase II with X and Y chromosomes associated in a 
pseudobivalent. Empty arrowheads indicate Y chromosome; empty arrows indicate X chromo­
some; solid arrows indicate largest autosomal pair. Bar represents 10 pm.
18 BRESSA, PAPESCHI and LARRAMENDY
are seldom observed. Mean chiasma frequency in 
cells at diakinesis-metaphase I varies from 5.33 to 
6.20 (mean = 5.75 ± 0.25) (Table 1). Though with 
different frequency among the specimens 
analysed, cells with one pair of univalents were 
observed (8.47%), derived in most of the cases 
from the largest autosomal pair (57.69%).
DISCUSSION
So far, the cytogenetic analysis of 26 species 
belonging to the Tygaeinae reveal a chromosome 
diploid number that varies from 12 to 22, with a 
sex chromosome determining system XY/XX, 
except Arocatus suboeneus which shows a multi­
ple system X1X2Y/X1X1X2X2 (UESHIMA and 
ASHLOCK 1980). Moreover, only five species of 
Lygaeus have been cytogenetically analysed, 
namely L. equestris (SCHACHOW 1932; PFALER- 
COLLANDER 1941), L. kalmii kalmii (UESHIMA 
and Ashlock 1980), L. turcicus (Wilson 1905), 
L. simulus (Parshad 1957) and L. alboornatus 
(present study). With the exception of L. alboor­
natus and L. simulus, cytogenetic reports from the 
remaining three species agree in demonstrating 
that they show a high homogeneity at the chro­
mosomal level. They share a diploid chromosome 
number of 14, and chromosomes do not differ 
much in their size. The sex chromosomes are the 
smallest of the complement, and more or less 
conspicuous differences between them have been 
reported. L. equestris is an extreme example since 
the Y chromosome is minute (WlLSON 1905; 
Schachow 1932; Pfaler-Collander 1941; 
Parshad 1957; Ueshima and Ashlock 1980). 
L. simulus is characterised by possessing a high 
chromosome number of 22, with two pairs of au­
tosomes larger than the remaining eight pairs 
which do not differ much in size among them­
selves; the sex chromosomes X and Y are also of 
similar size.
Ueshima and Ashlock (1980) have suggest­
ed that the modal diploid number for the sub­
family Tygaeinae is 14 (12+XY). Considering this 
modal karyotype as the ancestral one, the chro­
mosome complement of L. simulus should have 
originated through the fragmentation of four 
pairs of autosomes. Our results on L. alboorna­
tus reveal that this species shows the lowest 
number of elements for members of Tygaeinae. 
Taking in account the presence of a remarkable 
big-sized pair of autosomes in this species, it 
seems highly probable that its karyotype origi­
nated from the ancestral complement through 
one autosomal fusion.
Though the reduced number of individuals 
analysed, our results on L. alboomatus reveals the 
presence of ring bivalents at diakinesis-metaphase I. 
It is generally accepted that most Heteroptera 
possess as a rule only one chiasma per bivalent 
(UESHIMA 1979; Manna 1984); however, our pre­
sent observations in Lygaeus and previous find­
ings in other heteropteran species could indicate 
that the frequency of ring-shaped bivalents 
should be much higher than originally suggested 
(Camacho et al. 1985; Mola and Papeschi 1993; 
Bressa et al. 2001).
Uygaeids have relatively large chromosomes 
in regard to those observed in other heteropter­
an families. However, even with these large 
chromosomes, one exceptionally large autoso­
mal pair has been reported to be present in four 
subfamilies. Of these, the Henestarinae and 
Chauliopinae are known cytologically from sin­
gle species. In the Orsillinae and Blissinae, the 
extremely large chromosome is found in all but 
few species with a chromosome complement 
number of 14 elements while species with a 
higher number (usually 16) lack this chromo­
some. Accordingly, a fusion origin for this pe­
culiar pair of autosomes has been proposed 
(Ueshima and Ashlock 1980). Whether the re­
markable big-sized autosomal pair we observed 
in L. alboornatus is the same that the present in 
the former four subfamilies remains unknown, 
but we know, at least, that most probably they 
share the same origin through a similar fusion 
mechanism. A detailed analysis of the chromo­
somes involved in the formation of this peculiar 
pair of autosomes will be a fundamental step in 
our understanding of an important biological 
process. Furthermore, even when this peculiar 
and remarkable big-sized pair of autosomes is 
not homologous in these five subfamilies, its for­
mation and maintenance in the complement can 
be considered as a selectively neutral condition 
or at least, not a detrimental meiotic feature for 
the species.
Acknowledgements - This study was supported 
by the National Agency of Scientific and Techno­
logical Promotion (Contract grant number: BID 
802/OC-ARPICT No. 01-00000-00754), the Na­
tional Council of Scientific and Technological Re­
search (CONICET), the National University of La 
MEIOTIC CHROMOSOME BEHAVIOUR OF LYGAEUS ALBOORNATUS 19
Plata (Grant number 11/N324), and the National 
University of Buenos Aires (Grant number: TW01) 
from Argentina. The authors wish to thank Axel 
Bachmann Ph.D. for taxonomic identification of 
the specimens included in the study and the Buenos 
Aires Parks Administration from Argentina.
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Received September 4, 2001; accepted November 8, 2001


Meiotic studies in Lygaeus alboornatus Blanchard 1852 (Heteroptera, Lygaeidae, Lygaeinae)

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Meiotic studies in Lygaeus alboornatus Blanchard 1852 (Heteroptera, Lygaeidae, Lygaeinae)

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