Skip to main content
PMC home page
Comparative Cytogenetics logoLink to Comparative Cytogenetics
. 2015 Oct 7;9(4):625–644. doi: 10.3897/CompCytogen.v9i4.5371

Cytogenetic analyses of five amazon lizard species of the subfamilies Teiinae and Tupinambinae and review of karyotyped diversity the family Teiidae

Natália Dayane Moura Carvalho 1, Federico José Arias 2, Francijara Araújo da Silva 1, Carlos Henrique Schneider 1, Maria Claudia Gross 1
PMCID: PMC4698576  PMID: 26753079

Abstract Abstract

Lizards of the family Teiidae (infraorder Scincomorpha) were formerly known as Macroteiidae. There are 13 species of such lizards in the Amazon, in the genera Ameiva (Meyer, 1795), Cnemidophorus (Wagler, 1830), Crocodilurus (Spix, 1825), Dracaena (Daudin, 1801), Kentropyx (Spix, 1825) and Tupinambis (Daudin, 1802). Cytogenetic studies of this group are restricted to karyotype macrostructure. Here we give a compilation of cytogenetic data of the family Teiidae, including classic and molecular cytogenetic analysis of Ameiva ameiva (Linnaeus, 1758), Cnemidophorus sp.1, Kentropyx calcarata (Spix, 1825), Kentropyx pelviceps (Cope, 1868) and Tupinambis teguixin (Linnaeus, 1758) collected in the state of Amazonas, Brazil. Ameiva ameiva, Kentropyx calcarata and Kentropyx pelviceps have 2n=50 chromosomes classified by a gradual series of acrocentric chromosomes. Cnemidophorus sp.1 has 2n=48 chromosomes with 2 biarmed chromosomes, 24 uniarmed chromosomes and 22 microchromosomes. Tupinambis teguixin has 2n=36 chromosomes, including 12 macrochromosomes and 24 microchromosomes. Constitutive heterochromatin was distributed in the centromeric and terminal regions in most chromosomes. The nucleolus organizer region was simple, varying in its position among the species, as evidenced both by AgNO3 impregnation and by hybridization with 18S rDNA probes. The data reveal a karyotype variation with respect to the diploid number, fundamental number and karyotype formula, which reinforces the importance of increasing chromosomal analyses in the Teiidae.

Keywords: Macroteiidae, Chromosome, Heterochromatin, Differential staining, rDNA-FISH

Background

The family Teiidae is composed of lizards formerly known as macroteiids that are restricted to the New World (Giugliano et al. 2007, Harvey et al. 2012). Harvey et al. (2012) recently divided Teiidae in three subfamilies: (1) Teiinae, including the genera Ameiva (Meyer, 1795), Ameivula (Spix, 1825), Aurivela (Bell, 1843), Aspidoscelis (Fitzinger, 1843), Contomastix (Dumésil and Bibron, 1839), Cnemidophorus (Wagler 1830), Dicrodon (Dumésil and Bibron, 1839), Holcosus (Cope, 1862), Kentropyx (Spix, 1825), Medopheos (Bocourt, 1874) and Teius (Merrem, 1820); (2) Tupinambinae, including the genera Crocodilurus (Spix, 1825), Dracaena (Daudin, 1801), Salvator (Dumésil & Bibron, 1839) and Tupinambis (Daudin, 1802); and (3) Callopistinae, which contains the single genus Callopistes (Gravenhorst, 1837) (Harvey et al. 2012). However, the phylogenetic hypothesis of Teiidae based on molecular data (Reeder et al. 2002, Giugliano et al. 2007) differs substantially from the hypothesis proposed by Harvey et al. (2012).

Most chromosome data for teiid lizards refer only to the determination of diploid numbers and karyotype formulae (Fritts 1969, Gorman 1970, Lowe et al. 1970, Robinson 1973, Cole et al. 1979, de Smet et al. 1981, Navarro et al. 1981, Ward and Cole 1986, Cole et al. 1995, Markezich et al. 1997, Rocha et al. 1997, Walker et al. 1997, Manriquen-Moran et al. 2000, Veronese et al. 2003). Some species of this family have, however, been analyzed in detail with respect to their chromosomal structure and organization, as revealed by differential staining techniques, such as the detection of heterochromatin and nucleolar organizer regions (NORs), as well as chromosomal physical mapping of DNA sequences (Bickham et al. 1976, Bull 1978, Peccinini-Seale and Almeida 1986, Porter et al. 1991, Rocha et al. 1997, Veronese et al. 2003, Peccinini-Seale et al. 2004, Santos et al. 2007, Santos et al. 2008).

The family Teiidae can be divided into two chromosomal groups: the Dracaena group (currently the subfamily Tupinambinae), which has a karyotype with 34–38 chromosomes and a clear distinction of macrochromosomes (M) from microchromosomes (mi), and the Ameiva group (currently the subfamily Teiinae), which has a diploid number ranging from 46–56 chromosomes, with no distinction between macrochromosomes and microchromosomes (Gorman 1970).

We did a cytogenetic study of five species in the family Teiidae (Ameiva ameiva (Linnaeus, 1758), Cnemidophorus sp.1, Kentropyx calcarata (Spix, 1825), Kentropyx pelviceps (Cope, 1868) and Tupinambis teguixin (Linnaeus, 1758)) using classical as well as molecular cytogenetic markers (conventional staining, heterochromatin patterns, NOR locations and chromosomal physical mapping of 18S rDNA sequences). Karyotype organization in the family is discussed.

Methods

Thirty-three specimens belonging to the subfamilies Teiinae and Tupinambinae were collected in the state of Amazonas, Brazil, in the following localities: the riverside forests of the Jatapu river, the city of São Sebastião do Uatumã (0°50' - 01°55'S; 58°50' - 60°10'W), the Darahá and Ayuanã rivers, both in the city of Santa Isabel do Rio Negro (0°24'24"N; 65°1'1"W), the city of Manaus (3°07'13.03"S; 60°01'440"W) and the Purus riverside in the city of Tapauá (5°42'115"S; 63°13'684"W). All of the collections were conducted with permission from the Brazilian Environmental Protection Agency (ICMBio/SISBIO 41825-1). The collection sites are located in public lands (Table 1, Figure 1). The animals were euthanized soon after capture in the field with a lethal dose of the anesthetic sodium thiopental to avoid being deprived of food or water. This research was approved by the Ethics Committee for Animal Experimentation of the (UFAM) (number 041/2013). No endangered or protected species were used in this research study. The animals underwent cytogenetic procedures and were then fixed with 10% formaldehyde (injected in the coelom and digestive tract), preserved in 70% alcohol. Voucher specimens were deposited in the Herpetological Collection of the (INPA H31712, 33213, 34791, 34841, 35018).

Table 1.

Species of the Teiinae and Tupinambinae subfamilies: collection sites, number and the analyzed animals and voucher specimens (lots) are listed. AM.

Subfamily Species Collection sites Number and sex the analyzed animals Voucher specimens (lots)
Ameiva ameiva São Sebastião do Uatumã, AM Santa Isabel do Rio Negro, AM Tapauá, AM 11 (four males;
three females;
four without sex identification)		 INPA H33213
Cnemidophorus sp.1 Manaus, AM 13 (five males; eight females) INPA H35018
Teiinae Kentropyx calcarata São Sebastião do Uatumã, AM 4 (three males; one females) INPA H31712
Kentropyx pelviceps Tapauá, AM 3 (three females) INPA H34841
Tupinambinae Tupinambis teguixin São Sebastião do Uatumã, AM Tapauá, AM 3 (two females; one without sex identification) INPA H34791
Open in a new tab

Figure 1.

Figure 1.

Open in a new tab

Satellite image of the Amazon basin showing the three different geographical areas; 1 = São Sebastião do Uatumã; 2 = Santa Isabel do Rio Negro; 3 = Tapauá; 4 = Manaus.

Cellular suspensions were obtained from the bone marrow was removed soon after the euthanasia of animals in the field using an in vitro colchicine treatment (Ford and Hamerton 1956). (CH) was detected using barium hydroxide (Sumner 1972) and the NORs were detected using silver nitrate staining (Howell and Black 1980).

Genomic DNA was extracted from muscle tissue using a phenol-chloroform protocol (Sambrook and Russell 2001) and quantified using a NanoDrop 2000 spectrophotometer (Thermo Scientific). 18S rDNA was amplified by (PCR) using primers 18Sf (5’-CCG CTT TGG TGA CTC TTG AT-3’) and 18Sr (5’-CCG AGGACC TCA CTA AAC CA-3’) (Gross et al. 2010). PCR reactions were performed on a final volume of 15 µL, containing genomic DNA (200 ng), 10× buffer with 1.5 mM of MgCL2, Taq DNA polymerase (5 U/µL), dNTPs (1 mM), forward and reverse primers (5 mM) and Milli-Q water. The amplification cycles followed these steps: 1 min at 95 °C; 35 cycles of 1 min at 94 °C, 1 min at 56 °C, 1 min 30 s at 72 °C and 5 min at 72 °C.

The PCR product of the 18S rDNA was labeled with digoxigenin-11-dUTP (Dig- Nick Translation mix; Roche), by nick translation according to the manufacturer’s instructions. The antibody anti-digoxigenin rhodamine (Roche) was used for probing the signal. Homologue (DNA probes from the same species) and heterologue (probes of one species hybridized to the chromosome of another) hybridizations were made under stringency conditions of 77% (2.5 ng/µL of 18S rDNA, 50% formamide, 10% dextran sulfate, and 2× SSC at 37 °C for 18 h) (Pinkel et al. 1986). The chromosomes were counterstained with DAPI (2 mg/ml) in VectaShield mounting medium (Vector). The chromosomes were analyzed using an Olympus BX51 epifluorescence microscope and the images were captured with a digital camera (Olympus DP71) using Image-Pro MC 6.3 software. Mitotic metaphases were processed in Adobe Photoshop CS4 software and were measured using program ImageJ software. Chromosomes were organized by decreasing size, and chromosome morphology was determined based on the arm ratio for metacentric (m), submetacentric (sm), subtelocentric (st) and acrocentric (a) chromosomes (Levan et al. 1964). The karyotype formula was determined according to chromosomes that show a gradual series of acrocentric chromosomes, number of biarmed chromosomes, number of uniarmed chromosomes and number of macrochromosomes (M), and microchromosomes (mi) (Lowe and Wright 1966, Peccinini-Seale 1981). Macrochromosomes and microchromosomes are chromosomes that can be differentiated according to size; macrochromosomes are large and have one or two chromosome arms; microchromosomes are small (0.5–1.5 μm), puntiform and do not have any specific chromosome morphology.

Results

The diploid number for all specimens of Ameiva ameiva, Kentropyx calcarata and Kentropyx pelviceps was 50 chromosomes, and the karyotypic formula was classified by a gradual series of acrocentric chromosomes (Fig. 2a, i and m). Cnemidophorus sp.1 had 48 chromosomes with 2 biarmed chromosomes, 24 uniarmed chromosomes and 22 microchromosomes (Fig. 2e). Tupinambis teguixin had 36 chromosomes with 12 macrochromosomes (M) and 24 microchromosomes (mi). Pairs 1, 3, 4 and 5 of the macrochromosomes were metacentric and pairs 2 and 6 were submetacentric chromosomes (Fig. 3a). A secondary constriction was observed in the distal region of the long arms of pair 1 in Cnemidophorus sp.1, Kentropyx calcarata and Kentropyx pelviceps and in pair 2 in Tupinambis teguixin (Figs 2e, i, m and 3a). No differentiated sex chromosomes were observed in the analysed species.

Figure 2.

Figure 2.

Open in a new tab

Karyotypes of species belonging to Teiinae: a, e, i, m in conventional Giemsa staining b, f, j, n Regions of heterochromatin evidenced by C-band technique c, g, k, o highlight the nucleolar pair impregnated with AgNO3 d, h, l, p highlighted in the chromosome pair bearing the site of 18S rDNA (red) and chromosomes were counterstained with DAPI. m = Macrochromossome, mi = microchromossome. Scale bar = 10 µm.

Figure 3.

Figure 3.

Open in a new tab

Karyotype of Tupinambis teguixin: a in conventional Giemsa staining b Regions of heterochromatin evidenced by C-band technique c highlight the nucleolar pair impregnated with AgNO3 d highlight the chromosome pair bearing the site of 18S rDNA (red) and chromosomes were counterstained with DAPI. m = Macrochromossome, mi = microchromossome. Scale = 10 µm.

Constitutive heterochromatin was observed in the centromeric and terminal regions in most chromosomes of Ameiva ameiva, Cnemidophorus sp.1, Kentropyx calcarata and Kentropyx pelviceps (Figs 2b, f, j, n). In Tupinambis teguixin, heterochromatic blocks were located in the centromeric region of all the macrochromosomes. However, tenuous blocks were observed in the terminal regions in macrochromosomes and microchromosomes (Fig. 3b).

The NORs were located in the terminal region of the long arms of pair 7 in Ameiva ameiva (Fig. 2c). In Cnemidophorus sp.1, Kentropyx calcarata and Kentropyx pelviceps, NORs were seen in the distal region of the long arms of pair 1 and in pair 2 in Tupinambis teguixin, coincident with the secondary constriction present in the karyotypes of these species (Figs 2g, k, o and 3c, respectively). Fluorescent in situ hybridization (FISH) with an 18S rDNA probe revealed a chromosome pair bearing this site, coincident with the NOR sites in all of the five analyzed species (Figs 2d, h, l, p and 3d).

Discussion

Since the 1970s, cytogenetic analysis of the family Teiidae has shown that individuals could be categorized into two groups: the Ameiva group, with diploid number varying from 30–56 chromosomes, with no distinction between macrochromosomes and microchromosomes, and the Dracaena group, with a karyotype varying from 34–38 chromosomes, with a clear distinction between macrochromosomes and microchromosomes (Gorman 1970). By the end of the 1980s, several osteological and morphological studies corroborated the chromosomal data, thus supporting these two groups, which were subsequently considered subfamilies (Estes et al. 1988): Teiinae (Ameiva group) and Tupinambinae (Dracaena group).

Most karyotype data comes from species of the subfamily Teiinae, with descriptions of diploid numbers for 63 species. The karyotypes reveal a diploid number varying from 2n=30 in Ameiva auberi (Cocteau, 1838) to 2n=54 in Teius oculatus (D’orbigny & Bibron, 1837) and Teius teyou (Daudin, 1802), besides the presence of sex chromosomes of XX/XY in Aspidocelis tigris tigris (Baird & Girard, 1852) and Ameivula littoralis (Rocha, Bamberg Araújo, Vrcibradic, 2000). Some Aspidoscelis species show triploid numbers such as Aspidoscelis tessalatus (Say, 1823) with 69 chromosomes. Interspecific hybridization has been observed in some species of the genus Aspidoscelis, which were previously placed within the genus Cnemidophorus (Lowe et al. 1970, Walker et al. 1997, Lutes et al. 2010, Manriquez-Morán et al. 2000). Although the Ameiva group proposed by Gorman (1970) corresponds to the subfamily Teiinae, some species have a distinction between macrochromosomes and microchromosomes, while most chromosomes are acrocentric. This finding is contrary to what was proposed by Gorman (1970) as a cytogenetic feature of the Ameiva group (Table 2).

Table 2.

Basic cytogenetic data compiled from the literature for the Teiidae family. (2n), (KF), (FN). Three descriptions of karyotypic formulas: (a) number of biarmed chromosomes, number of uniarmed chromosomes and number of microchromosomes; (b) chromosomes that show a gradual series of acrocentric chromosomes; (c) macrochromosome chromosomes (M) and microchromosomes (mi). For data not included in the literature, “-” is indicated.

Subfamily Genus Species (sensu [2]) Species (initial description) 2n Type of KF and description FN Reference
Callopistinae Callopistes Callopistes flavipunctatus Callopistes flavipunctatus 2n=38 c (12M+26m) 50 2
Callopistes maculatus Callopistes maculatus 2n=38 c (12M+26m) 26, 50 2, 8
Teiinae Ameiva Ameiva ameiva Ameiva ameiva 2n=50 a (0: 26: 24)
b (gradual series of acrocentric chromosomes)		 50 2, 18
Tupinambinae Ameiva auberi Ameiva auberi 2n=30 a (8: 10:12) 38 11
Ameiva chrysolaema Ameiva chrysolaema 2n=50 a (0: 22: 28), (6: 20: 24) 50, 56 2
Ameiva dorsalis Ameiva dorsalis 2n=50 a (4: 22: 24) 54 2
Ameiva exsul Ameiva exsul 2n=50 a (0: 26: 24) 50 2
Ameiva maynardi Ameiva maynardi 2n=50 a (4: 22: 24) 54 2
Ameivula Ameivula nativo
Ameivula litorralis
Ameivula ocellifera 		Cnemidophorus nativo
Cnemidophorus littoralis
Cnemidophorus ocellifera 		2n=50
2n=46 (XX/XY)
2n=50		 a (5: 19: 24)
a (5: 19: 22)
b(gradual series of acrocentric chromosomes)		 53
51
-		 14
9
18
Aspidoscelis Aspidoscelis angusticeps Cnemidophorus angusticeps 2n=44, 46 a (6: 20: 18), a (2: 24: 20) 50, 48 3, 16
Aspidoscelis burti Cnemidophorus burti 2n=46 a (2: 24: 20) 48 3
Aspidoscelis calidipes Cnemidophorus calidipes 2n=46 a (2: 24: 20) 48 3
Aspidoscelis ceralbensis Cnemidophorus ceralbensis 2n=52 - - 4
Aspidoscelis communis Cnemidophorus communis 2n=46 a (2: 24:20) 48 3
Aspidoscelis costatus Cnemidophorus costatus 2n=46 a (2: 24:20) 48 3
Aspidoscelis cozumelae Cnemidophorus cozumelae 2n=49, 50 a (0: 28: 21), a (11: 19: 20) 49, 61 3, 16
Aspidoscelis deppei Cnemidophorus deppei 2n=50, 52 a (0: 26: 24), a (0: 28: 24) 50, 52 3, 16
Aspidoscelis exsanguis Cnemidophorus exsanguis 3n=69* - - 3, 10
Aspidoscelis flagellicaudas Cnemidophorus flagellicaudas 3n=69* - - 3
Aspidoscelis gularis Cnemidophorus gularis 2n=46 a (2: 24: 20) 48 3
Aspidoscelis guttatus Cnemidophorus guttatus 2n=52 a (0: 28: 24) 52 3
Aspidoscelis hyperythrus Cnemidophorus hyperythrus 2n=52 a (0: 28: 24) 52 3
Aspidoscelis inoratus Cnemidophorus inoratus 2n=46 a (2: 24: 20) 48 3, 10
Aspidoscelis laredoensis Cnemidophorus laredoensis 2n=46 a (2: 24: 20) 48 4
Aspidoscelis lineatissima Cnemidophorus lineatissima 2n=52 a (0: 28: 24) 52 3
Aspidoscelis marmoratus Cnemidophorus marmoratus 2n=46 a (0: 22: 24) 46 11
Aspidoscelis maslini Cnemidophorus maslini 2n=47 a (14: 13: 20) 49 3
Aspidoscelis mexicana Cnemidophorus mexicana 2n=46 a (2: 24: 20) 48 3
Aspidoscelis motaguae Cnemidophorus motaguae 2n=46 a (2: 24: 20) 48 3
Aspidoscelis neomexicanus Cnemidophorus neomexicanus 2n=46 a (4: 20: 22) 50 3,10
Aspidoscelis opatae Cnemidophorus opatae 3n=69* - - 3
Aspidoscelis parvisocius Cnemidophorus parvisocius 2n=46 a (2: 24: 20) 48 3
Aspidoscelis rodecki Cnemidophorus rodecki 2n=50 - - 1
Aspidoscelis sacki Cnemidophorus sacki 2n=46 a (2: 24: 20) 48 3
Aspidoscelis sptemvittatus Cnemidophorus sptemvittatus 2n=46 a (2: 24: 20) 48 3
Aspidoscelis sexlineatus Cnemidophorus sexlineatus 2n=46 a (2: 24: 20), a (8: 18: 20) 48, 54 3, 5
Aspidoscelis sonorae Cnemidophorus sonorae 2n=46, 3n=69* a (4: 20: 22) 48 2, 3, 10
Aspidoscelis tesselatus Cnemidophorus tesselatus 2n=46, 3n=69* a (4: 20: 22) 50 3, 10, 15
Aspidoscelis tigris tigris Cnemidophorus tigris tigris 2n=46(XX/XY) a (6: 16: 24) 52 2, 10
Aspidoscelis tigris aethiops Cnemidophorus tigris aethiops 2n=46 a (6: 16: 24) 52 3
Aspidoscelis tigris estebanensis Cnemidophorus tigris estebanensis 2n=46 a (6: 16: 24) 52 3
Aspidoscelis tigris gracilis Cnemidophorus tigris gracilis 2n=46 a (6: 16: 24) 52 3
Aspidoscelis tigris marmoratus Cnemidophorus tigris marmoratus 2n=46 a (6: 16: 24) 52 3
Aspidoscelis tigris maximus Cnemidophorus tigris maximus 2n=46 a (6: 16: 24) 52 3
Aspidoscelis tigris septentrionalis Cnemidophorus tigris septentrionalis 2n=46 a (6: 16: 24) 52 3
Aspidoscelis ubiparens Cnemidophorus uniparens 3n=69* - - 3, 10
Aspidoscelis velox Cnemidophorus velox 3n=69* - - 3
Cnemidophorus Cnemidophorus arenivagus Cnemidophorus arenivagus 2n=50 a (2: 24: 24) 52 9, 13
Cnemidophorus arubensis Cnemidophorus arubensis 2n=50 a (2: 24: 24) 52 9, 13
Cnemidophorus cryptus Cnemidophorus cryptus 2n=50 - 52 9
Cnemidophorus gramivagus Cnemidophorus gramivagus 2n=50 - 52 9
Cnemidophorus lemniscatus Cnemidophorus lemniscatus 2n=50 a (2: 24: 24) 52 2, 3
Cnemidophorus murinus Cnemidophorus murinus 2n=50 a (2: 24:24) 52 4, 3
Contomastix Contomastix lacertoides Cnemidophorus lacertoides 2n=50 a (0: 26: 24) 52 6, 17
Kentropyx Kentropyx borckiana Kentropyx borckiana 2n=50 a (0: 26: 24) 50 12
Kentropyx calcarata Kentropyx calcarata 2n=50 b(gradual series of acrocentric chromosomes) 50 12, 19
Kentropyx striata Kentropyx striata 2n=50 a (0: 26: 24) 50 12
Kentropyx paulensis Kentropyx paulensis 2n=50 b(gradual series of acrocentric chromosomes) 50 18
Kentropyx pelviceps Kentropyx pelviceps 2n=50 b(gradual series of acrocentric chromosomes) 50 20
Kentropyx vanzoi Kentropyx vanzoi 2n=50 b(gradual series of acrocentric chromosomes) 50 18
Teius Teius oculatus Teius oculatus 2n=54 a (8: 28: 18) 62 17
Teius teyou Teius teyou 2n=54 a (8: 22: 24) 62 2
Crocodilurus - Crocodilurus lacertinus 2n=34 c (12M+22m) 46 2
Crocodilurus amazonicus Crocodilurus amazonicus 2n=34 c (12M+22m) 46 19
Dracaena Dracaena guianensis
 Dracaena guianensis
 2n=38
 a (10:2:26) 48
 2
Tupinambis - Tupinambis nigropunctatus 2n=36, 38 a (10: 2: 24), c (16M+22m) 46, 54 2, 7
Tupinambis quadrilineatus Tupinambis quadrilineatus 2n=38 c (12M+26m) - 19
Tupinambis teguixin Tupinambis teguixin 2n=38, 36 a (10: 0: 28), (12M+24m) 48 7, 19
Salvator Salvator merianae Tupinambis merianae 2n=36, 38 a (10: 0: 26), c (12M+26m) 48, 50 7, 17, 19
Open in a new tab

Ameiva ameiva and Kentropyx calcarata, which belong to Teiinae, have the same diploid number (2n=50 chromosomes). This result corroborates the available data for these species from different localities (Gorman 1970, Beçak et al. 1972, Peccinini-Seale and Almeida 1986, Schmid and Guttenbach 1988, Sites et al. 1990, Veronese et al. 2003, Santos et al. 2007). However, in present study Ameiva ameiva and Kentropyx calcarata present a gradual series of acrocentric chromosomes characterized by absence of distinction between macrochromosomes and microchromosomes, similar to the results described by Cole et al. (1995) and Santos et al. (2007). The same finding is observed for Kentropyx pelviceps, whose cytogenetic characteristics are revealed for the first time in the present study.

Furthermore, karyotypic formulae composed of biarmed chromosomes, uniarmed chromosomes and microchromosomes has been described for Ameiva ameiva and Kentropyx calcarata and in the other species genera of the subfamily Teiinae (Lowe and Wright 1966, Gorman 1970, Beçak et al. 1972, Peccinini-Seale and Almeida 1986, Schmid and Guttenbach 1988, Sites et al. 1990, Veronese et al. 2003). These data show that some differences may result from different classification parameters adopted by several authors in their chromosomal analyses.

Currently, the genus Cnemidophorus is divided into four morphological groups: (1) Cnemidophorus lemniscatus including the species Cnemidophorus arenivagus (Markezich, Cole & Dessauer, 1997), Cnemidophorus arubensis (Lidth de Jeude, 1887), Cnemidophorus cryptus (Cole & Dessauer, 1993), Cnemidophorus flavissimus (Ugueto, Harvey & Rivas, 2010), Cnemidophorus gramivagus (Mccrystal & Dixon, 1987), Cnemidophorus lemniscatus espeuti (Boulenger, 1885), Cnemidophorus lemniscatus gaigei (Ruthven, 1924), Cnemidophorus lemniscatus lemniscatus (Linnaeus, 1758), Cnemidophorus lemniscatus splendidus (Markezich, Cole & Dessauer, 1997), Cnemidophorus pseudolemniscatus (Cole & Dessauer, 1993), Cnemidophorus senectus (Ugueto, Harvey & Rivas, 2010) and Cnemidophorus sp. B.; (2) Cnemidophorus nigricolor including the species Cnemidophorus leucopsammus (Ugueto & Harvey, 2010), Cnemidophorus nigricolor (Peters, 1873), Cnemidophorus rostralis (Ugueto & Harvey, 2010) and Cnemidophorus sp. A; (3) Cnemidophorus murinus including the species Cnemidophorus murinus (Laurenti, 1768) and Cnemidophorus ruthveni (Burt, 1935) and (4) Cnemidophorus vanzoi including the species Cnemidophorus vanzoi (Baskin & Williams, 1966) (Harvey et al. 2012). It is noteworthy that several new species of this genus have been described, showing that the taxonomy of this genus has not yet been elucidated, which emphasizes the need for morphological and molecular studies in this genus. Cytogenetically, some species of Cnemidophorus have 50 chromosomes, composed of biarmed chromosomes, uniarmed chromosomes and microchromosomes (Table 2, Peccinini-Seale and Almeida 1986). However, the karyotype of Cnemidophorus sp.1 from Manaus, in Amazonas state, differs from those described for other species of the genus. This species has 2n = 48 chromosomes with the absence of a pair of microchromosomes (Table 2, present study). Non-robertsonian chromosomal rearrangements may be associated with chromosomal evolution of this genus, which favored changes in diploid number (reduction in diploid number). Another population in Amazonas state (county Manacapuru) identified as belonging to Cnemidophorus lemniscatus group has the expected diploid number of 50 chromosomes with the presence of biarmed chromosomes and uniarmed microchromosomes (0:26:24) (Sites et al. 1990). Our results show that the specimens we sampled from Manaus are karyotypically distinct from specimens we sampled from Manacapuru so Cnemidophorus sp.1 (Cnemidophorus lemniscatus group) could represent a new species.

Seven species from the subfamily Tupinambinae, have had their karyotypes analyzed, with diploid numbers varying from 2n=34–38 chromosomes, with the presence of both macrochromosomes and microchromosomes (Santos et al. 2008, present study). No sex chromosome system has been documented in the subfamily (Gorman 1970). Tupinambis teguixin has 2n=36 chromosomes (12M+24m) (Table 2) the same number and karyotype formula was found by other authors (Gorman 1970, de Smet et al. 1981, Santos et al. 2008). Beçak et al. (1972) described a diploid number of 38 chromosomes (12M+26m) for Tupinambis teguixin, with an additional pair of microchromosomes.

In the family Teiidae, heterochromatic blocks are located in the centromeric and terminal regions of almost all chromosomes. In some chromosomes, heterochromatic blocks are present in the pericentromeric, interstitial and terminal regions (Table 3). In the five species of the family Teiidae analyzed in this study, we observed a significant number of heterochromatic blocks in the centromere and terminal regions in the most of the chromosomes, which is consistent with similar patterns described in the literature.

Table 3.

Cytogenetic banding data compiled from the literature for the differential Teiidae family. (NORs), (CH), (FISH). Locality: (AM), (BA), (USA), (ES), (GO), (MT), (MG), (PA), (RJ), (RS), (RO), (SP), (SE), (TO). For data not included in the literature, “-” is indicated.

Subfamily Species
(Current description)		 Species
(Initial description)		 Locality NOR CH FISH Reference
Teiinae Ameiva ameiva Ameiva ameiva GO, RO, MT, TO Terminal region of the long arms of pair 7 Centromeric and terminal regions - 8
Ameiva ameiva Ameiva ameiva AM Terminal region of the long arms of pair 7 Centromeric and terminal regions 18S rDNA (pair 7) Present work
Ameiva auberi Ameiva auberi - - - 45S rDNA (pair of microchromosomes) 4
Aspidoscelis gularis Cnemidophorus gularis USA Centromeric region - 1
Aspidoscelis laredoensis Cnemidophorus laredoensis USA - Centromeric region - 1
Aspidoscelis marmoratus Cnemidophorus marmoratus - - - 45S rDNA (pair 2) 4
Aspidoscelis sexlineatus Cnemidophorus sexlineatus USA - Centromeric region - 1
Aspidoscelis tigris Cnemidophorus tigriss USA - Centromeric region - 2
Ameivula littoralis
Ameivula nativo
Ameivula ocellifera 		Cnemidophorus littoralis
Cnemidophorus nativo
Cnemidophorus ocellifera 		RJ
ES
BA, SE, MG		 Terminal region of the long arms of pair 8
Multiple NORs
(not indicated pairs)
Terminal region of the long arms of pair 5		 -
-
Centromeric and terminal regions		 -
-
-		 7
5
8
Cnemidophorus arenivagus Cnemidophorus arenivagus - Terminal region of the long arms of pair 1
 - - 3
Cnemidophorus cryptus Cnemidophorus cryptus - Terminal region of the long arms of pair 1 - - 3
Cnemidophorus gramivagus Cnemidophorus gramivagus - Terminal region of the long arms of pair 1 - - 3
Cnemidophorus lemniscatus Cnemidophorus lemniscatus - Terminal region of the long arms of pair 1 - - 3
Cnemidophorus sp.1 - AM Terminal region of the long arms of pair 1 Centromeric and terminal regions 18S rDNA (pair 1) Present work
Contomastix larcetoides Cnemidophorus larcetoides RS - Centromeric region - 6
Kentropryx calcarata Kentropryx calcarata BA, TO, MT Distal region of the long arms of pair 1 - - 8
Kentropryx calcarata Kentropryx calcarata AM Distal region of the long arms of pair 1 Centromeric and terminal regions 18S rDNA (pair 1) Present work
Kentropryx paulensis Kentropryx paulensis SP Distal region of the long arms of pair 1 Centromeric and terminal regions - 8
Kentropyx pelviceps Kentropyx pelviceps AM Distal region of the long arms of pair 1 Centromeric and terminal regions 18S rDNA (pair 1) Present work
Kentropryx vanzoi Kentropryx vanzoi RO Distal region of the long arms of pair 1 - - 8
Teius oculatus Teius oculatus RS Multiple NORs (not indicated pairs) - - 6
Tupinambinae Crocodilurus amazonicus Crocodilurus amazonicus PA Distal region of the long arms of pair 2 Pericentromeric region - 9
Salvator meriane Tupinambis merianae TO, SP, ES Distal region of the long arms of pair 2 Pericentromeric region - 9
Tupinambis quadrilineatus Tupinambis quadrilineatus GO, TO Distal region of the long arms of the pair 2 Centromeric, pericentromeric, interstitial, proximal and terminal regions - 9
Tupinambis teguixin Tupinambis teguixin GO, TO Distal region of the long arms of pair 2 - - 9
Tupinambis teguixin Tupinambis teguixin AM Distal region of the long arms of pair 2 Centromeric and terminal regions 18S rDNA (pair 2) Present work
Open in a new tab

The heterochromatin patterns for Cnemidophorus sp.1, Kentropyx calcarata, Kentropyx pelviceps and Tupinambis teguixin are described for the first time in this study. The heterochromatin distributional pattern is similar among the analyzed species, suggesting a common pattern for species in the family Teiidae. Three species in the subfamily Tupinambinae (Crocodilurus amazonicus (Spix, 1825), Salvator merianae (Duméril & Bibron, 1839) and Tupinambis quadrilineatus (Manzani & Abe, 1997), however, show species-specific heterochromatin patterns, with heterochromatic blocks in the centromeric, pericentromeric, interstitial and proximal regions of most chromosomes (Santos et al. 2008). The existence of such a distinctive pattern can likely be attributed to the addition of heterochromatin or the heterochromatization process during the evolution of these species. Heterochromatic regions are rich in repetitive DNA sequences usually located in the centromeric or terminal regions of chromosomes. This has often been considered important species-specific or population markers (Carvalho et al. 2012, Schneider et al. 2013). Even though heterochromatin may be located on the same chromosome region in different species, this does not mean it has the same genetic composition, which may differ in the amount of repetitive DNA sequences in the chromosomes (Chaiprasertsri et al. 2013).

Although the five species in the family Teiidae analyzed in the present study present a conserved karyotype macrostructure, some chromosomal characteristics differentiate the karyotype of these species. In Cnemidophorus sp.1, Kentropyx calcarata, Kentropyx pelviceps and Tupinambis teguixin, the presence of a secondary constriction localized in the distal region of pairs 1 and 2 was observed. The secondary constriction is absent in Ameiva ameiva.

Secondary constrictions are typically present in a single chromosomal pair and are very common in several lizard species (Bertolloto et al. 1996, Kasahara et al. 1996, Bertolloto et al. 2002, Srikulnath et al. 2009a). This region contain genes that produce ribosomal RNA and these regions may hold nucleoli proteins during the entire process of cellular division (Guerra 1988). In such secondary constrictions, NORs are usually placed and they are identified, indirectly, by silver nitrate impregnation of the chromosomes. Such impregnation marks only nucleoli proteins involved in the transcriptional activity of ribosomal genes of the 45S family. NORs may be located in a single chromosomal pair, a basal characteristic already reported for different lizard species (Porter et al. 1991).

In the present study, the localization of the NORs was revealed as an genus marker and this information has already been discussed for some genera in the family Teiidae, such as Kentropyx (Kentropyx calcarata, Kentropyx paulensis (Boettger, 1893) and Kentropyx vanzoi Gallagher & Dixon, 1980), Crocodilurus (Crocodilurus amazonicus), Cnemidophorus (Cnemidophorus arenivagus, Cnemidophorus cryptus, Cnemidophorus gramivagus and Cnemidophorus lemniscatus lemniscatus), Salvator (Salvator merianae) and Tupinambis (Tupinambis quadrilineatus and Tupinambis teguixin). Localization of the NORs is important for characterizing species and evolutionary studies among teiid lizards (Santos et al. 2007, 2008).

Tupinambis teguixin has a simple NOR, as evidenced by the secondary constriction of the long arm of pair 2. A common characteristic among species the subfamily Tupinambinae is the presence of such a secondary constriction in pair 2 (Gorman 1970). Four species of the subfamily Teiinae, Ameiva ameiva, Cnemidophorus sp.1, Kentropyx calcarata and Kentropyx pelviceps, also have simple NORs, but they are located in distinct chromosomal pairs. In Cnemidophorus sp.1, Kentropyx calcarata and Kentropyx pelviceps, a secondary constriction was seen in pair 1 while in Ameiva ameiva occurred in pair 7. The NOR data analyzed for Ameiva ameiva and Kentropyx calcarata in the present study corroborate previous data (Schmid and Guttenbach 1988, Cole et al. 1995, Veronese et al. 2003, Santos et al. 2007), but for Cnemidophorus sp.1 and Kentropyx pelviceps they are new data.

Two populations of Ameiva ameiva from the eastern Amazon showed multiple NORs involving pairs 1, 2, 6, 16, 18, 19 and some small chromosomes (Peccinini-Seale and Almeida 1986). Some authors suggest that the inter-individual variation observed in Ameiva ameiva may be related to the identification of active NOR sites, once the silver nitrate binds to acid nucleoli proteins involved with the transcriptional activity of the ribosomal genes (Miller et al. 1976, Howell and Black 1980, Boisvert et al. 2007). Such variability may also result from impregnation of CH regions rich in acid residues, in which the nitrate impregnates both the NORs and heterochromatic regions not bearing ribosomal sites, thereby not revealing the exact number of NORs (Sumner 2003). Moreover, this variation may be suggesting that Ameiva ameiva is a specie complex, as other teiids like Ameivula ocellifera (Spix, 1825) (Arias et al. 2011) or Cnemidophorus lemniscatus (Harvey et al. 2012).

Using 45S ribosomal DNA probes and FISH, it is possible to understand the organization of the NORs and to elucidate questions concerning the chromosomal organization and karyotypic evolution. The FISH technique is a more refined method than silver nitrate impregnation to locate 45S rDNA sequences in mitotic chromosomes (Carvalho et al. 2012, Terencio et al. 2012, Schneider et al. 2013). However, for the species analyzed in the present study, the fluorescent in situ hybridization of the 18S ribosomal gene corroborated the results obtained with silver nitrate impregnation, confirming the existence of this ribosomal site in a single pair of chromosomes. This same pattern was identified in other species in the family Teiidae, supporting the sites seen in a microchromosome pair in Ameiva auberi (Cocteau, 1838). In Aspidoscelis marmorata (Baird & Girard, 1852), the same pattern was located in a macrochromosome pair (Porter et al. 1991). Furthermore, it was possible to observe a size heteromorphism of the sites between the homologue chromosomes in the four analyzed species, a fact also described for other lizard species (O’Meally et al. 2009, Srikunath et al. 2009b, Srikunath et al. 2011). Such a size heteromorphism is likely associated with unequal crossing-over mechanisms, rearrangements such as transpositions, deletions and/or duplications or variations in the number of rDNA copies present in such regions that would entail some changes in ribosomal sites (Gross et al. 2010, Ribeiro et al. 2008).

Conclusion

Our present data and those from the literature show that teiid lizards have karyotype variation with respect to diploid number, fundamental number and karyotype formula. This, reinforces the importance to increase the number of chromosomal analyses in the family Teiidae. Studies are currently underway with the chromosomal physical mapping of repetitive DNA sequences in three species of Amazonian teiids that are essential for the understanding of genome organization and karyotype evolution in this group of lizards.

Acknowledgments

This work was supported by the Universidade Federal do Amazonas (UFAM), the graduate program of INPA Genética, Conservação e Biologia Evolutiva, Rede BioPHAM (CNPq/FAPEAM grant number: 563348/2010-0); Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (grant number: 474617/2013-0); FAPEAM (020/2013); CAPES (Pró-Amazônia – grant number 23038.009447/2013-45, 3295/2013). Species were collected with a permit issued by the Chico Mendes Institute for Biodiversity Conservation (ICMBio/SISBIO license number 41825-1). NDMC received funding from the Fundação de Amparo a Pesquisas do Estado do Amazonas. The authors are grateful to Sergio Marques de Souza for revision of the manuscript and Dra. Eliana Feldberg for the epifluorescence microscope. American Manuscript Editors reviewed this paper.

Citation

Carvalho NDM, Arias FJ, da Silva FA, Schneider CH, Gross MC (2015) Cytogenetic analyses of five amazon lizard species of the subfamilies Teiinae and Tupinambinae and review of karyotyped diversity the family Teiidae. Comparative Cytogenetics 9(4): 625–644. doi: 10.3897/CompCytogen.v9i4.5371

References

  1. Arias F, Carvalho CM, Rodrigues MT, Zaher H. (2011) Two new species of Cnemidophorus (Squamata: Teiidae) from the Caatinga, northwest of Brazil. Zootaxa 2787: 37–54. [Google Scholar]
  2. Beçak ML, Beçak W, Denaro L. (1972) Chromosome polymorphism, geographical variation and karyotypes in Sauria. Caryologia 25: 313–326. doi: 10.1080/00087114.1972.10796485 [Google Scholar]
  3. Bertolotto CEV, Rodrigues MT, Skuk G, Yonenaga-Yassuda Y. (1996) Comparative cytogenetic analysis with differential staining in three species of Liolaemus (Squamata, Tropiduridae). Hereditas 125: 257–264. doi: 10.1111/j.1601-5223.1996.00257.x [Google Scholar]
  4. Bertolotto CEV, Pellegrino KCM, Rodrigues MT, Skuk G, Yonenaga-Yassuda Y. (2002) Comparative cytogenetics and supernumerary chromosomes in the Brazilian lizard genus Enyalius (Squamata, Polychrotidae). Hereditas 136: 51–57. doi: 10.1034/j.1601-5223.2002.1360108.x [DOI] [PubMed] [Google Scholar]
  5. Bickham JW, McKinney CO, Michael MF. (1976) Karyotypes of the parthenogenetic whiptail lizard Cnemidophorus laredoensis and its presumed parental species (Sauria: Teiidae). Herpetologica 4: 395–399. [Google Scholar]
  6. Boisvert FM, Koningsbruggen SV, Navascués J, Lamond AI. (2007) The multifunctional nucleolus. Molecular and Cellular Biology 8: 574–585. doi: 10.1038/nrm2184 [DOI] [PubMed] [Google Scholar]
  7. Bull JJ. (1978) Sex chromosome differentiation: an intermediate stage in a lizard. Canadian Journal of Genetics and Cytology 20: 205–209. doi: 10.1139/g78-023 [Google Scholar]
  8. Carvalho NDM, Gross MC, Schneider CH, Terencio ML, Zuanon J, Feldberg E. (2012) Cytogenetics of Synbranchiformes: a comparative analysis of two Synbranchus Bloch, 1795 species from the Amazon. Genetica 140: 149–158. doi: 10.1007/s10709-012-9666-5 [DOI] [PubMed] [Google Scholar]
  9. Cole CJ, MacCoy A, Achaval F. (1979) Karyotype from a South American teiid lizard, Cnemidophorus lacertoides. American Museum Novitates 2617: 1–5. [Google Scholar]
  10. Cole CJ, Dessauer HC, Townsend CR, Arnold MG. (1995) Kentropyx borckiana (Squamata, Teiidae): a unisexual lizard of hybrid origin in the Guiana region, South America. American Museum Novitates 3145: 1–30. [Google Scholar]
  11. Chaiprasertsri N, Uno Y, Peyachoknagul S, Prakhongcheep O, Baicharoen S, Charernsuk S, Nishida C, Matsuda Y, Koga A, Srikulnath K. (2013) Highly species-specific centromeric repetitive DNA sequences in lizards: molecular cytogenetic characterization of a novel family of satellite DNA sequences isolated from the water monitor lizard (Varanus salvator macromaculatus, Platynota). Journal of Heredity 104: 798–806. doi: 10.1093/jhered/est061 [DOI] [PubMed] [Google Scholar]
  12. de Smet WH. (1981) Description of the orcein stained karyotypes of 36 lizard species (Lacertilia, Reptilia) belonging to the families Teiidae, Scincidae, Lacertidae, Cordylidae and Varanidae (Autarchoglossa). Acta Zoologica et Pathologica Antverpiensia 76: 73–118. [Google Scholar]
  13. Estes R, Queiroz K, Gauthier J. (1988) Phylogenetic relationships within Squamata. In: Phylogenetic relationships of the lizard families. Stanford University Press, California, 119–281. [Google Scholar]
  14. Ford CE, Hamerton JL. (1956) The chromosomes of man. Nature 178: 1020–1023. doi: 10.1038/1781020a0 [DOI] [PubMed] [Google Scholar]
  15. Fritts T. (1969) The systematics of the parthenogenetic lizards of the Cnemidophorus cozumela complex. Copeia 1969: 519–535. doi: 10.2307/1441932 [Google Scholar]
  16. Giugliano LG, Collevatti RG, Colli GR. (2007) Molecular dating and phylogenetic relationships among Teiidae (Squamata) inferred by molecular and morphological data. Molecular Phylogenetics and Evolution 45: 168–179. doi: 10.1016/j.ympev.2007.05.017 [DOI] [PubMed] [Google Scholar]
  17. Gorman GC. (1970) Chromosomes and the systematics of the family Teiidae (Sauria: Reptilia). Copeia 1970: 230–245. doi: 10.2307/1441645 [Google Scholar]
  18. Guerra M. (1988) Introdução à citogenética geral. Editora Guanabara, Rio de Janeiro, Brasil. [Google Scholar]
  19. Gross MC, Schneider CH, Valente GT, Martins C, Feldberg E. (2010) Variability of 18S rDNA locus among Symphysodon fishes: chromosomal rearrangements. Journal of Fish Biology 76: 1117–1127. doi: 10.1111/j.1095-8649.2010.02550.x [DOI] [PubMed] [Google Scholar]
  20. Harvey MB, Ugueto GN, Gutberlet Jr RL. (2012) Review of Teiid Morphology with a Revised Taxonomy and Phylogeny of the Teiidae (Lepidosauria: Squamata). Zootaxa 3459: 1–156. [Google Scholar]
  21. Howell WM, Black DA. (1980) Controlled silver staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 3: 1014–1015. doi: 10.1007/BF019538557 [DOI] [PubMed] [Google Scholar]
  22. Kasahara S, Pellegrino KCM, Rodrigues MT, Yonenaga-Yassuda Y. (1996) Comparative cytogenetic studies of eleven species of the Tropidurus torquatus group (Sauria, Tropiduridae), with banding patterns. Hereditas 125: 37–46. doi: 10.1111/j.1601-5223.1996.00037.x [Google Scholar]
  23. Levan A, Fredga K, Sandberg AA. (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52: 201–220. doi: 10.1111/j.1601-5223.1964.tb01953.x [Google Scholar]
  24. Lowe CH, Wright JW. (1966) Chromosomes and karyotypes of Cnemidophorus teiid lizards. Mammalia Chromosome Newslettr 22: 199–200. [Google Scholar]
  25. Lowe CH, Wright JW, Cole CJ, Bezy RL. (1970) Chromosomes and evolution of the species groups of Cnemidophorus (Reptilia: Teiidae). Journal of Zoological Systematics and Evolutionary Research 2: 128–141. doi: 10.2307/2412450 [Google Scholar]
  26. Lutes AA, Neaves WB, Baumann DP, Wiegraebe W, Baumann P. (2010) Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature 464: 283–287. doi: 10.1038/nature08818 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Manríquez-Morán NL, Villagrán-Santa Cruz M, Cruz Méndez-De La Cruz FR. (2000) Origin and evolution of the parthenogenetic lizards, Cnemidophorus maslini and C. cozumela. Journal of Herpetology 4: 634–637. doi: 10.2307/1565287 [Google Scholar]
  28. Markezich AL, Cole CJ, Dessauer HC. (1997) The blue and green whiptail lizards (Squamata, Teiidae, Cnemidophorus) of the Peninsula de Paraguana, Venezuela: systematics, ecology, descriptions of two new taxa, and relationships to whiptails of the Guianas. American Museum Novitates 3207: 1–60. [Google Scholar]
  29. Miller EA, Dev VG, Tantravahi R, Miller OJ. (1976) Supression of human nucleolus organizer activity in mouse human somatic hybrid cells. Experimental Cell Research 101: 235–243. doi: 10.1016/0014-4827(76)90373-6 [DOI] [PubMed] [Google Scholar]
  30. Navarro J, Sallaberry M, Veloso A, Valencia J. (1981) Diversidad cromossômica em lagartos (Squamata – Sauria). I Advances citotaxonomicos. Perspectiva de estudios evolutivos em Iguanidae. Meio Ambiente 5: 28–38. [Google Scholar]
  31. O’Meally D, Miller H, Patel HR, Marshall Graves JA, Ezaz T. (2009) The first cytogenetic map of the Tuatara, Sphenodon punctatus. Cytogenetics and Genome Research 127: 213–223. doi: 10.1159/000300099 [DOI] [PubMed] [Google Scholar]
  32. Peccinini-Seale D. (1981) New developments in vertebrate cytotaxonomy IV. Cytogenetic studies in reptiles. Genetica 56: 123–148. doi: 10.1007/BF00055413 [Google Scholar]
  33. Peccinini-Seale D, Almeida TMB. (1986) Chromosomal variation nucleolar organizers and constitutive heterochromatin in the genus Ameiva and Cnemidophorus (Sauria, Teiidae). Caryologia 39: 227–239. doi: 10.1080/00087114.1986.10797785 [Google Scholar]
  34. Peccinini-Seale D, Rocha CFD, Almeida TMB, Araújo AFB, De Sena MA. (2004) Cytogenetics of the brazilian whiptail lizard Cnemidophorus littoralis (Teiidae) from a resting area (Barra de Marica) in Southeastern Brazil. Brazilian Journal of Biology 64: 661–667. doi: 10.1590/S1519-69842004000400014 [DOI] [PubMed] [Google Scholar]
  35. Pinkel D, Straume T, Gray JW. (1986) Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proceedings of the National Academy of Sciences 83: 2934–2938. doi: 10.1073/pnas.83.9.2934 [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Porter CA, Meredith JH, Sites JW Jr, Baker RJ. (1991) Location of ribosomal DNA in chromosomes of squamate reptiles: systematic and evolutionary implications. Herpetologica 27: 271–280. [Google Scholar]
  37. Presch W. (1974) Evolutionary relationships and biogeography of the macroteiid lizards (Family Teiidae, Subfamily Teiinae). Bulletin Southern California Academy of Sciences 73: 23–32. [Google Scholar]
  38. Presch W. (1983) The lizard family Teiidae: is it a monophyletic group? Zoological Journal of the Linnean Society 77: 189–197. doi: 10.1111/j.1096-3642.1983.tb00529.x [Google Scholar]
  39. Reeder TW, Cole CJ, Dessauer HC. (2002) Phylogenetic relationships of whiptail lizards of the genus Cnemidophorus (Squamata:Teiidae): attest of monophyly, reevaluation of karyotypic evolution, and review of hybrid origins. American Museum Novitates 3365: 1–61. doi: 10.1206/0003-0082(2002)365<0001:PROWLO>2.0.CO;2 [Google Scholar]
  40. Ribeiro LB, Matoso DA, Almeida MC, Vicari MR, Moraes-Neto A, Svidinicki MCCM, Artoni RF. (2008) Karyotypic variability in Iheringichthys labrosus (Teleostei, Pimelodidae) from the Tibagi River basin (Paraná State, Brazil). Genetics and Molecular Research 7: 718–724. doi: 10.4238/vol7-3gmr456 [DOI] [PubMed] [Google Scholar]
  41. Robinson MD. (1973) Chromosomes and systematics of the Baja California whiptail lizards Cnemidophorus hyperythrus and C. ceralbensis (Reptilia: Teiidae). Journal of Zoological Systematics and Evolutionary Research 22: 30–35. doi: 10.2307/2412375 [Google Scholar]
  42. Rocha CFD, Bergallo HG, Peccinini-Seale D. (1997) Evidence of an unisexual population of the Brazilian whiptail lizard genus Cnemidophorus (Teiidae), with description of a new species. Herpetologica 53: 374–382. [Google Scholar]
  43. Santos RML, Pellegrino KCM, Rodrigues MT, Yonenaga-Yassuda Y. (2007) Banding patterns and chromosomal evolution in five species of neotropical Teiinae lizards (Squamata: Teiidae). Genetica 131: 231–240. doi: 10.1007/s10709-006-9133-2 [DOI] [PubMed] [Google Scholar]
  44. Santos RML, Rodrigues MT, Yonenaga-Yassuda Y, Pellegrino KCM. (2008) Differential staining and microchromosomal variation in karyotypes of four Brazilian species of Tupinambinae lizards (Squamata: Teiidae). Genetica 134: 261–266. doi: 10.1007/s10709-007-9233-7 [DOI] [PubMed] [Google Scholar]
  45. Sambrook J, Russell DW. (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, New York, 633–664. [Google Scholar]
  46. Sites JW, Peccinini-Seale DM, Mortiz C, Wright JW, Brown WM. (1990) The evolutionary history of parthenogenetic Cnemidophorus lemniscatus (Sauria: Teiidae) I. Evidence for a hybrid origin. Evolution 44: 906–921. doi: 10.2307/2409554 [DOI] [PubMed] [Google Scholar]
  47. Sumner AT. (1972) A simple technique for demonstrating centromeric heterochromatin. Experimental Cell Research 75: 304–306. doi: 10.1016/0014-4827(72)90558-7 [DOI] [PubMed] [Google Scholar]
  48. Sumner AT. (2003) Chromosomes: organization and function. Blackwell Publishing, New York. [Google Scholar]
  49. Schmid M, Guttenbach M. (1988) Evolutionary diversity of reverse (R) fluorescent chromosomes bands in vertebrates. Chromosoma 97: 101–114. doi: 10.1007/BF00327367 [DOI] [PubMed] [Google Scholar]
  50. Schneider CH, Gross MC, Terencio ML, Artoni RF, Vicari MR, Martins C, Feldberg E. (2013) Chromosomal evolution of neotropical cichlids: the role of repetitive DNA sequences in the organization and structure of karyotype. Reviews in Fish Biology and Fisheries 23: 201–214. doi: 10.1007/s11160-012-9285-3 [Google Scholar]
  51. Srikulnath K, Nishida C, Matsubara K, Uno Y, Thongpan A, Suputtitada S, Apisitwanich S, Matsuda Y. (2009a) Karyotypic evolution in squamate reptiles: comparative gene mapping revealed highly conserved linkage homology between the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Lacertilia) and the Japanese four-stripedrat snake (Elaphe quadrivirgata, Colubridae, Serpentes). Chromosome Research 17: 975–986. doi: 10.1007/s10577-009-9101-7 [DOI] [PubMed] [Google Scholar]
  52. Srikulnath K, Matsubara K, Srikulnath K, Uno Y, Thongpan A, Suputtitada S, Apisitwanich S, Matsuda Y, Nishida C. (2009b) Karyological characterization of the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Squamata) by molecular cytogenetic approach. Cytogenetic and Genome Research 125: 21–223. doi: 10.1159/000230005 [DOI] [PubMed] [Google Scholar]
  53. Srikulnath K, Uno Y, Matsubara K, Thongpan A, Suputtitada S, Apisitwanich S, Nishida C, Matsuda Y. (2011) Chromosomal localization of the 18S-28S and 5S rRNA genes and (TTAGGG)n sequences of butterfly lizards (Leiolepis belliana belliana and Leiolepis boehmei, Agamidae, Squamata). Genetics and Molecular Biology 34: 582–586. doi: 10.1590/S1415-47572011005000042 [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Terencio ML, Schneider CH, Gross MC, Nogaroto V, de Almeida MC, Artoni RF, Vicari MR, Feldberg E. (2012) Repetitive sequences associated with differentiation of W chromosome in Semaprochilodus taeniurus. Genetica 140: 505–512. doi: 10.1007/s10709-013-9699-4 [DOI] [PubMed] [Google Scholar]
  55. Veronese LB, Freitas TRO, Krause L. (2003) Cytogenetic studies of four brazilian species of teiid lizards (Squamata, Teiidae). Caryologia 56: 107–114. doi: 10.1080/00087114.2003.10589313 [Google Scholar]
  56. Walker JM, Cordes JE, Taylor HL. (1997) Parthenogenetic Cnemidophorus tesselatus complex (Sauria: Teiidae): a neotype for diploid C. tesselatus (Say, 1823), redescription of the taxon, and description of a mew triploid species. Herpetologica 53: 233–259. [Google Scholar]
  57. Ward OG, Cole CJ. (1986) Nucleolar dominance in diploid and triploid parthenogenetic lizards of hybrid origin. Cytogenetics and Cell Genetics 42: 177–182. doi: 10.1159/000132274 [Google Scholar]

Articles from Comparative Cytogenetics are provided here courtesy of Pensoft Publishers

RESOURCES