Cytogenetic studies of the family Lycosidae (Arachnida: Araneae) are scarce. Less than 4% of the described species have been analyzed and the male haploid chromosome numbers ranged from 8+X 1 X 2 to 13+X 1 X 2 . Species formerly classified as Lycosa were the most studied ones. Our aim in this work was to perform a comparative analysis of the meiosis in " Lycosa " erythrognatha Lucas, " Lycosa " pampeana Holmberg and Schizocosa malitiosa (Tullgren). We also compared male and female karyotypes and characterized the heterochromatin of " L. " erythrognatha . The males of the three species had 2n = 22, n = 10+X 1 X 2 , all the chromosomes were telocentric and there was generally a single chiasma per bivalent. In " Lycosa " pampeana , which is described cytogenetically for the first time herein, the bivalents and sex chromosomes showed a clustered arrangement at prometaphase I. The comparison of the male/female karyotypes (2n = 22/24) of " Lycosa " erythrognatha revealed that the sex chromosomes were the largest of the complement and that the autosomes decreased gradually in size. The analysis of the amount, composition and distribution of heterochromatin with C-banding and staining with DAPI- and CMA 3 - showed that " Lycosa " erythrognatha had little GC-rich heterochromatin in the pericentromeric region of all chromosomes. In addition, the actual occurrence of the genus Lycosa in the Southern Hemisphere is discussed.
meiosis; C-banding; fluorochrome staining; karyotype; spiders; "Lycosa" and Schizocosa
Cytogenetic studies of three Lycosidae species from Argentina (Arachnida, Araneae)
María A. Chemisquy1
Sergio G. Rodríguez Gil2
Cristina L. Scioscia3
Liliana M. Mola2,4
1Instituto de Botánica Darwinion, San Isidro, Buenos Aires, Argentina
2Laboratorio de Citogenética y Evolución, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina
3División Aracnología, Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Ciudad Autónoma de Buenos Aires, Argentina
4Consejo Nacional de Investigaciones Científicas y Técnicas, Ciudad Autónoma de Buenos Aires, Argentina
Cytogenetic studies of the family Lycosidae (Arachnida: Araneae) are scarce. Less than 4% of the described species have been analyzed and the male haploid chromosome numbers ranged from 8+X1 X 2 to 13+X1 X 2. Species formerly classified as Lycosa were the most studied ones. Our aim in this work was to perform a comparative analysis of the meiosis in "Lycosa" erythrognatha Lucas, "Lycosa" pampeana Holmberg and Schizocosa malitiosa (Tullgren). We also compared male and female karyotypes and characterized the heterochromatin of "L." erythrognatha. The males of the three species had 2n = 22, n = 10+X1X2, all the chromosomes were telocentric and there was generally a single chiasma per bivalent. In "Lycosa" pampeana, which is described cytogenetically for the first time herein, the bivalents and sex chromosomes showed a clustered arrangement at prometaphase I. The comparison of the male/female karyotypes (2n = 22/24) of "Lycosa" erythrognatha revealed that the sex chromosomes were the largest of the complement and that the autosomes decreased gradually in size. The analysis of the amount, composition and distribution of heterochromatin with C-banding and staining with DAPI- and CMA3 - showed that "Lycosa" erythrognatha had little GC-rich heterochromatin in the pericentromeric region of all chromosomes. In addition, the actual occurrence of the genus Lycosa in the Southern Hemisphere is discussed.
Cytogenetic studies of the family Lycosidae (Arachnida, Araneae) are scarce and were performed in less than 4% of the 2324 known species (Platnick, 2008). Most of the analyzed species had only telocentric or acrocentric chromosomes, which ranged from 2n = 18, n = 8+X1X2 (male) to 2n = 28/30 (male/female), n = 13+X1X2 (male). The 2n = 28/30, which is present in 50% of the analyzed species, is probably the modal diploid number of the family. The sex chromosome mechanism X1X2/X1X1X2X2 (male/female) occurs in 94% of the lycosid species and is considered as an ancestral trait in spiders. The derived systems are: X0 in Lycosabarnesi, L. nordenskjoldi, Wadicosa quadrifera and an unidentified species of Schizocosa (Schizocosa sp. 2 in Table 1); X1X2X3 in an unidentified species of Lycosa (Lycosa sp. 8 in Table 1), and a neo-XY system with multiple X chromosomes in Pardosa morosa (Král, 2004). Most cytological studies have been performed in species formerly classified as Lycosa and the most common male haploid chromosome number was n = 13+X1X2 in the Northern Hemisphere species. The Southern Hemisphere species presented complements with n = 10+X1X2 (males) or derived from it (Table 1).
The content, distribution and composition of the constitutive heterochromatin in spiders have been poorly analyzed (Brum-Zorrilla and Cazenave, 1974; Brum-Zorrilla and Postiglioni, 1980; Rowell, 1985; Datta and Chatterjee, 1988; Rowell, 1991; Gorlova et al., 1997; Silva et al., 2002; Araujo et al., 2005a, 2005b; Rodríguez Gil et al., 2007). The first characterization of heterochromatin in spiders was performed in Schizocosa malitiosa using C-banding. All chromosomes showed small pericentromeric heterochromatic bands in this species and in all the other Lycosidae analyzed (Brum-Zorrilla and Cazenave, 1974; Brum-Zorrilla and Postiglioni, 1980; Gorlova et al., 1997).
Morphological and molecular phylogenetic studies questioned the taxonomic position of a number of species currently placed in Lycosa (sensu lato) (including Lycosa erythrognatha), since they appear not to be closely affiliated with Lycosa tarantula (Linnaeus 1758), the type species of the genus (Murphy et al., 2006; Álvares and Brescovit, 2007). In view of this uncertainty, we named the species with its original combination, but with the generic name inside inverted commas.
In this work we analyzed and compared the meiotic behavior of “Lycosa” erythrognatha Lucas 1836, “Lycosa” pampeana Holmberg 1876 and Schizocosamalitiosa (Tullgren 1905). We used C-banding, DAPI- and CMA3-staining to analyze the male and female karyotypes and the amount, composition and distribution of the heterochromatin in “L.” erythrognatha. We compared our results with those reported for other lycosid species. A literature review of the cytogenetics Lycosidae and a discussion on the actual occurrence of the genus Lycosa in Southern Hemisphere are also included.
Figure 2 Meiosis in “Lycosa” erythrognatha (2n = 22, n = 10+X1X2 and n = 10): (a) spermatogonial prometaphase; (b) zygotene; (c) pachytene; (d) early diplotene; (e) late diplotene with two univalents (arrows) and a bivalent with two chiasmata (arrowhead); (f) diakinesis; (g) metaphase I; (h) anaphase I; (i) telophase I; (j) metaphase II with sex chromosomes; (k) anaphase II with sex chromosomes; (l) telophase II without sex chromosomes. The arrowheads point to the sex chromosomes. Bar = 10 μm.
Figure 3 Testicular cells of “Lycosa” erythrognatha (2n = 22 = 20+X1X2) after staining with CMA3 (a, c, e, f) and with DAPI (b, d): (a-b) spermatogonial prometaphase; (c-d) pachytene; (e) diakinesis; (f) metaphase I. The arrowheads point to the sex chromosomes; the V points to CMA3 bright bands and the asterisk marks the DAPI dull regions. Bar = 10 μm.
Figure 4 Meiosis of “Lycosa” pampeana male (n = 10+X1X2 and n = 10): (a) pachytene; (b) diplotene; (c) diakinesis; (d-f) prometaphase I; (g) telophase I; (h) prometaphase II with sex chromosomes; (i) telophase II without sex chromosomes. The arrowheads point to the sex chromosomes. Bar = 10 μm.
Figure 5 Meiosis in Schizocosa malitiosa (2n = 22, n = 10+X1X2 and n = 10): (a) spermatogonial prometaphase; (b) pachytene; (c) diplotene with a bivalent with two chiasmata; (d) diakinesis; (e) metaphase I; (f) anaphase I; (g) telophase I; (h) metaphase II with sex chromosomes; (i) metaphase II without sex chromosomes; (j) telophase II with sex chromosomes. The arrowheads point to the sex chromosomes. Bar = 10 μm.
We analyzed 21 males and nine females of “Lycosa” erythrognatha from Buenos Aires City and surroundings (34°48' S - 58°41' W) (17 males, five females), Martín García Island Natural Preserve (34°18' S - 58°24' W, Buenos Aires Province) (two males), Magdalena (35°08' S - 57°51' W, Buenos Aires Province) (one female), Parque Nacional “El Palmar” (24°08' S - 64°58' W, Entre Ríos Province) (one female), Malargüe (35°48' S - 69°59' W, Mendoza Province) (one male, two females) and Posadas (27°40' S - 55°93' W, Misiones Province) (one male); four males of “Lycosa” pampeana from Buenos Aires City and surroundings; and seven males of Schizocosa malitiosa from Martín García Island Natural Preserve (one male), Gualeguaychú (33°04' S - 58°43' W, Entre Ríos Province) (three males, one subadult male), San Juan Poriahú (27°61' S - 56°98' W, Corrientes Province) (one male) and Embalse de Río Tercero (32°17' S - 64°25' W, Córdoba Province) (one male).
Adult males and females were collected in the field and reared at the Arachnology Division of the Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” (MACN). Voucher specimens were deposited in the National Collection of Arachnology (MACN-Ar, Cristina Scioscia).
For male meiotic analyses, testes were dissected out and kept in 3:1 ethanol:acetic acid at 4 °C. Preparations were obtained by squashing in iron propionic haematoxylin.
Fluorescent staining with 4'-6-diamidino-2-phenylindole (DAPI) and chromomycin A3 (CMA3) was carried out on unstained chromosomes. After squashing a piece of testis in 45% acetic acid, the coverslip was removed with the dry-ice method and slides were air-dried. The sequential DAPI-CMA3 staining was performed according to Rebagliati et al. (2003).
For the mitotic analysis specimens of “Lycosa” erythrognatha were injected with 0.1 mL of a 0.01% colchicine solution. After 1.25 h, several drops of haemolymph were removed from the coxal joints and the gonads together with some digestive tissues were dissected. Each sample was suspended in 2 mL of hypotonic solution (KCl 0.56%) for 15 min, centrifuged at 800 rpm for 5 min, and fixed in 1 mL of 3:1 ethanol:acetic acid. The cell suspension was dropped onto clean slides, air-dried and stained with Giemsa for chromosome counting and karyotyping. C-banding was carried out according to Sumner (1972).
Chromosome measurements were performed in twelve well-spread mitotic metaphases using the MicroMeasure version 3.3 software (Reeves and Tear, 2000). The total haploid complement length (TCL) in females was calculated by adding the mean value of each chromosome pair (in arbitrary units). In males, the TCL was calculated after the analysis of the relative length of all chromosomes, which was used to identify those having no homologues (sex chromosomes). The male and female idiograms were drawn based on the length of each chromosome pair in relation to the TCL. Chromosomes were also measured with a vernier caliper in order to estimate the TCL in microns.
The diploid number in somatic cells was 22 in males and 24 in females. All the chromosomes were telocentric (Figures 1 a and bFigure 1 “Lycosa” erythrognatha chromosomes (2n = 22): male (a) and female (b) karyograms; C-banded male metaphase (c); relative chromosome sizes in the male (d). Bar = 10 μm. ). The X1 and X2 were the largest chromosomes of the complement, with 12.83% and 11.69% of the TCL, respectively, whereas the autosomes decreased gradually in size, with the largest and smallest pairs representing 9.54% and 5.47% of the TCL, respectively (Figures 1 a, b and dFigure 1 “Lycosa” erythrognatha chromosomes (2n = 22): male (a) and female (b) karyograms; C-banded male metaphase (c); relative chromosome sizes in the male (d). Bar = 10 μm. ). The total haploid complement length (TCL) was 43.8 μm, the sex chromosomes were 5.03 + 0.04 μm and 4.78 + 0.1 μm long and the autosomes ranged between 4.13 + 0.25 μm and 2.64 + 0.09 μm. C-banding revealed the presence of small positive bands in the pericentromeric region of all chromosomes (Figure 1cFigure 1 “Lycosa” erythrognatha chromosomes (2n = 22): male (a) and female (b) karyograms; C-banded male metaphase (c); relative chromosome sizes in the male (d). Bar = 10 μm. ).
“Lycosa” erythrognatha (2n = 22, n = 10+X1X2 and n = 10)
At spermatogonial prometaphases and metaphases the sex chromosomes and the autosomes were isopycnotic (Figure 2a). At prophase I, up to pachytene, the sex chromosomes were positively heteropycnotic and closely associated (Figures 2 b and c). The sex chromosomes were usually isopycnotic from diakinesis onwards, but appeared negatively heteropycnotic in some cells; in both cases they remained associated and differed in size (Figure 2d-f). Bivalents had a single proximal or interstitial chiasma (Figure 2d-g; 3e-f), but two chiasmata could occasionally be observed in one of the largest bivalents (Figure 2e). In six individuals, a pair of medium-sized autosomal univalents were seen in a low frequency at diakinesis (less than 10% of the cells) and two univalent pairs were seen in a single cell (Figure 2e). The sex chromosomes were located apart from the bivalents at metaphase I (Figures 2g; 3f) and precociously migrated together towards the same pole at anaphase I (Figure 2h-i). This resulted in two types of metaphase II, one with ten autosomes and the other with ten autosomes plus the X1X2 chromosomes (Figure 2j). The sister chromatids of each sex chromosome were always closely associated, whereas the autosomal chromatids were only associated by the centromeric region (Figure 2j). The sex chromosomes and autosomes migrated simultaneously and were positioned slightly apart at anaphase II (Figure 2k) resulting in cells with ten autosomes (Figure 2l) and with ten chromosomes plus X1X2 in telophase II. An atypical meiosis was observed in some cells of all the males (unpublished data).
Sequential DAPI-CMA3-staining of spermatogonial prometaphases and metaphases revealed that all the pericentromeric C-positive bands were bright after CMA3-staining and showed no differential fluorescence with DAPI (Figure 3a-b). The sex chromosomes were brightly fluorescent after DAPI- and CMA3-staining at early prophase I. The CMA3-bright bands observed in mitotic chromosomes were composed of several smaller CMA3-fluorescent bands at pachytene. The same bands were generally dull after DAPI-staining (Figure 3c-d). A single pericentromeric CMA3-bright band could be observed in the autosomes and sex chromosomes from diplotene onwards (Figure 3e-f).
“Lycosa” pampeana (2n = 22, n = 10+X1X2, n = 10)
The sex chromosomes were positively heteropycnotic and closely associated at early prophase I (Figure 4a) and turned isopycnotic at diakinesis, when they remained associated and showed different sizes. All autosomal bivalents presented a single proximal or distal chiasma and bivalents with two chiasmata were never found (Figure 4b-c). Bivalents adopted a particular disposition during prometaphase I, with some of them (from one to four) lining up on the equatorial plate and the others located near the poles. The sex chromosomes were either in the cell equator or at one pole (Figure 4d-f). The bivalents and sex chromosomes lined up on the equatorial plane at metaphase I and the sex chromosomes migrated together to the same pole at anaphase I (Figure 4g). Two types of prometaphases II and metaphases II could be distinguished, one with ten and the other with 12 chromosomes (Figure 4h). Chromosomes with a telocentric morphology were clearly seen at anaphase I and II (Figures 4 g and i).
Schizocosa malitiosa (2n = 22, n = 10+X1X2, n = 10)
Twenty-two isopycnotic chromosomes were seen in spermatogonial prometaphases and metaphases (Figure 5a). The sex chromosomes were closely associated and positively heteropycnotic at early prophase I (Figure 5b) and turned isopycnotic from diakinesis onwards, when they were close to each other and showed different sizes (Figure 5c-d). Most of the bivalents had a single interstitial or distal chiasma, and less frequently a proximal one, as could be seen at metaphase I (Figure 5e). Some cells also presented one bivalent with two distal chismata (Figure 5c). The sex chromosomes were not lined up on the equatorial plate at metaphase I, but closer to one pole (Figure 5e), and they migrated together to the same pole at anaphase I (Figure 5f). The sex chromosomes remained condensed and positively heteropycnotic at prophase II (Figure 5g) and were similar in size to the largest autosomes at metaphase II. The sister chromatids of the X1 and X2 chromosomes were always associated, whereas autosomal chromatids were only associated by their centromeric region (Figure 5h-i). The chromosomes of this species were also telocentric (Figure 5h-j).
Only ten species of Lycosidae from South America have been cytogenetically studied. Two of them belonged to the genus Schizocosa Chamberlin 1904 and the remaining eight to the genus Lycosa Latreille 1804 (Table 1). They were collected in Uruguay, Brazil and Argentina.
In this work, we found a 2n = 22 (20+X1X2, male) in Schizocosamalitiosa. This species had a karyotype with all telocentric chromosomes, with the sex chromosomes being the largest of the complement and chiasmata mainly at interstitial or distal positions. In populations of S. malitiosa from Uruguay, Brum-Zorrilla and Cazenave (1974) and Brum-Zorrilla and Postiglioni (1980) described 2n = 22 in males and 2n = 24 in females, telocentric chromosomes, sex chromosomes that were the smallest of the complement and bivalents with proximal chiasmata in the males. These results suggest that S. malitiosa is polytypic for the size of the sex chromosomes and chiasma position. In the males of an unidentified Schizocosa species (Schizocosa sp. 2 in Table 1) included within the “malitiosa group”, Postiglioni and Brum-Zorrilla (1981) found 2n = 23 (22+X), with a metacentric X chromosome probably resulting from the fusion of two telocentric X chromosomes. The five species from the USA already studied (S. communis, S. crassipes, S. ocreata, S. rovneri, S. stridulans) also had n = 10+X1X2, whereas an unidentified species from India (Schizocosa sp. 1 in Table 1) had n = 13+X1X2 (Painter, 1914; Hard, 1939; Mittal, 1960, 1963; Stratton, 1997). These results allowed us to conclude that the modal chromosome number for the genus is 2n = 22/24 (male/female) and that the sex chromosome determination system is of the X1X2/ X1X1X2X2 type.
The present work represents the first cytogenetic study conducted in “Lycosa” pampeana. This species had 2n = 22 (20+X1X2, male), with all telocentric chromosomes. At prometaphase I, the bivalents and the sex chromosomes were peculiarly arranged into three groups, one group being located on the equatorial plane and the remaining two at the cell poles. This very unusual chromosome disposition in spiders was formerly described for three species of Tegenaria (Agelenidae) by Revell (1947), who considered that it resulted from the primary polarization of the bivalents at early prophase I due to the attraction of the heterochromatic regions by the centrosome. When the centrosome began to split, each new centrosome acted as a polarization centre for bivalents, which gradually became aligned on the metaphase plate. This stage, named “transitional metaphase” by Revell (1947), resembles the prometaphases observed in “Lycosa” pampeana.
“Lycosa” erythrognatha had 2n = 22/24 (male/female), n = 10+X1X2, n = 10 in males, all telocentric chromosomes and the sex chromosomes were the largest of the complement. Bivalents usually had one chiasma, although bivalents with two chiasmata and univalents were occasionally seen and probably resulted from desynapsis. The number and location of the chiasmata during meiosis varied largely among cells. Such variation may be determined not only genetically, but also by environmental factors, both internal and external to the individual (John and Lewis, 1965; Jones, 1987; Appels et al., 1998). The presence of univalents and bivalents with two chiasmata in the same individual and even in the same cell may be a consequence of changes in the mechanisms regulating chiasma frequency and distribution. The chromosome number, some karyotypic features and the meiotic behavior herein observed in “Lycosa” erythrognatha are consistent with results obtained in specimens of the same species from Uruguay and Brazil (Díaz and Sáez, 1966a Díaz M., Sáez F.A. (1966a) Investigaciones citogenéticas sobre algunas especies de araneidos uruguayos. Anales II Congreso Latinoamericano de Zoología 1:São Paulo3-9. , 1966b Díaz M., Sáez F.A. (1966b) Karyotypes of South America Araneida. Mem Inst Butantan 33:153-154. ; Giroti et al., 2007).
“Lycosa” erythrognatha is characterized by scanty GC-rich heterochromatin located in the pericentromeric region of all chromosomes. The DAPI- and CMA3-bright fluorescence of the sex chromosomes during early prophase I is consistent with the allocycly of these chromosomes during male meiosis and probably reflects different degrees of chromatin condensation rather than differences in base composition. The heterochromatin content has only been characterized in other four species of the family. C-banding of Alopecosa albofasciata showed small blocks of pericentromeric heterochromatin in the autosomes and uniformly heterochromatic sex chromosomes during male meiosis (Gorlova et al., 1997). In Schizocosa malitiosa, Lycosa thorelli and in an unidentified species of Lycosa (Lycosa sp. 7 in Table 1), small AT-rich (Hoechst 33258 positive) C-positive bands were observed in the pericentromeric regions of all chromosomes. A few Hoechst-positive fluorescent bands found in the telomeric regions of some chromosomes of Lycosa sp. 7 (Table 1) were not C-positive (Brum-Zorrilla and Postiglioni, 1980). In the male meiosis of Schizocosa malitiosa, the sex chromosomes were strongly positively heteropycnotic (Brum-Zorrilla and Cazenave, 1974). The analysis of the heterochromatin content revealed that all the studied species of Lycosidae are characterized by a small amount of tandem repeated DNA sequences. On the other hand, there is some heterogeneity in heterochromatin composition, which can be summarized as follows: a) C-positive, AT-rich pericentromeric heterochromatin; b) C-positive, GC-rich pericentromeric heterochromatin, and c) AT-rich telomeric heterochromatin, undetectable with C-banding.
In a molecular phylogenetic reconstruction of the wolf spiders at the subfamily level, Murphy et al. (2006) stated that a number of species currently placed in Lycosa (sensu lato) (including “Lycosa” erythrognatha) do not form a clade and none of them appear to be closely affiliated with Lycosa tarantula (Linnaeus 1758), the type species of the genus; in contrast, “clades within the Lycosinae appear to reflect geographic regions rather than existing recognised morphological parameters”. The authors claimed that Australasian wolf spiders do not possess the defining features of Lycosa and that a critical study is necessary to determine their true taxonomic position.
The systematics of South American Lycosidae is poorly known and the taxonomic status of many of the species is far from being resolved. Most of the species originally described under the genus Lycosa were transferred to other genera on the basis of poor diagnostic morphological characters. Our karyological study supports previous morphological and behavioral evidence (unpublished data, two thesis works and congress presentations by several authors) indicating that “Lycosa” erythrognatha, “Lycosa” pampeana and a group of species from South America should be transferred to another genus (e.g.Schizocosa) or that they would belong to a new, still undescribed genus. Álvares and Brescovit (2007), based exclusively on morphological characters, proposed that these species, as well as Schizocosa malitiosa, should be transferred to Hogna Simon 1885.
It is outstanding that all the South American species so far analyzed had 2n = 22/24 (male/female) or complements almost certainly derived from it. Even though the number of cytogenetically analyzed Schizocosa and Hogna species is not representative for the group, all the Schizocosa species from the USA already studied presented n = 10+X1X2, while Hogna species from the USA had n = 13+X1X2 and n = 11+X1X2 (Table 1).
Cytogenetic analyses of other South American species currently classified within Lycosinae are needed. The information obtained will provide baseline data on the karyotypic evolution within each genus. It will be particularly relevant to formulate a new revision of the taxonomy and phylogeny of the group taking into account morphological, cytogenetical and molecular data. This revision could confirm, as was the case for Australasian wolf spiders (Murphy et al., 2006), that Lycosa does not occur in South America.
This study was supported by grants from the Buenos Aires University (UBA) to Dr L. Poggio and Dr L. M. Mola (Ex 317) and from the National Council of Scientific and Technological Research (CONICET) (PIP 5927 Poggio-Mola), and (PIP 5654 González-Scioscia). The authors thank Mr. Hernán Dinapoli for technical assistance and Prof. Gustavo Gagna for offering his house for specimen collections.
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Received: January 25, 2008; Accepted: May 8, 2008
Liliana María Mola. Laboratorio de Citogenética y Evolución, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes y Costanera Norte, C1428EHA, Ciudad Autónoma de Buenos Aires, Argentina. E-mail: email@example.com.
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