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Diversidad cromosomica en tuco-tucos (Ctenomys, Rodentia) de los humedales del noreste Argentino.

CHROMOSOMAL VARIABILITY IN TUCO-TUCOS (CTENOMYS, RODENTIA) FROM THE ARGENTINEAN NORTHEASTERN WETLANDS

INTRODUCTION

Subterranean rodents of the genus Ctenomys (commonly named tuco-tucos) have been considered a clear example of chromosomal evolution since the seminal work of Reig and Kiblisky (1969) because of their broad range of chromosomal numbers (from 2n = 10 to 70) (Cook et al., 1990; Ortells et al., 1990). Among mammals, the genus Ctenomys is characterized by having one of the highest numbers of living species, about 60 as registered by Woods y Kilpatrick (2005). Most of the species present quite distinctive karyotypes, a characteristic that was called to be an example of chromosomal speciation (Reig y Kiblisky, 1969). However, chromosomal polymorphisms or polytypisms also occur in Ctenomys. For instance, C. pearsoni is considered a single species although its karyotypes range between 2n = 56 to 2n = 70 as reviewed by Tomasco and Lessa (2007). Similar cases have been recently reported in the Brazilian tuco-tuco species C. lami (2n = 54 to 58) and C. minutus (2n = 42 to 50) that also depict large intraspecific karyotypical variability, mainly due to centric fusions/fissions and pericentric inversions (Freitas, 2007; Lopes et al., 2013).

The present work deals with chromosomal variability of the Ctenomys Corrientes group that exhibits one of the widest ranges of diploid numbers within the genus. Demes of tuco-tucos from this group are patchily distributed in a vast area under the wide influence of the Ibera marsh and its natural channels and lagoons, in the Argentinean province of Corrientes, between the Parana and Uruguay rivers. Sandy soils, predominant in this area, are favorable habitats for tuco-tucos, though their proximity to the wetlands makes these habitats temporary and spatially fragmented. The dynamics of habitat availability (via expansions and contractions) imposes putative contacts between neighboring populations and/or splitting and divergence of demes.

The pioneering works of Contreras y Scolaro (1986), Ortells et al. (1990) and Ortells y Barrantes (1994) initiated chromosomal studies in the Ctenomys Corrientes group. Ortells et al. (1990) showed that high karyotypical variability, with chromosomal numbers ranging from 2n = 42 to 2n = 70, characterized this group. Chromosomal numbers and morphology have been described for some karyomorphs in the mentioned contributions, as well as in subsequent ones (Garcia et al., 2000; Arguelles et al., 2001). However, for several karyomorphs only chromosomal (2n) and fundamental (FN) numbers have been published without any data on chromosomal morphology (Gimenez et al., 2002; Lanzone et al., 2007). The purpose of the present work is to expand the chromosomal information of the Ctenomys Corrientes group, particularly of the Ibera subgroup that comprises the tuco-tucos that inhabit the margins of the Ibera marsh (Caraballo et al., 2012). We found 3 new karyomorphs, described another 5 from which only 2n and FN values were available, and confirmed chromosome number and morphology of another 6 previously published karyomorphs.

MATERIALS AND METHODS

Specimens

This study included 47 individuals from 15 localities of the province of Corrientes (Argentina). Animals were live- captured with modified Oneida Victor Nr. 0 snap traps. Guidelines of the American Society of Mammalogists (Gannon et al., 2007) were followed. Well-preserved skulls were deposited in the Coleccion de Mastozoologia of the Museo Argentino de Ciencias Naturales "Bernardino Rivadavia". Trapping localities with their geographical location (Fig. 1) as well as field / catalog numbers (when available) were recorded: Estancia la Tacuarita (27[degrees] 58' 42.7" S; 56[degrees] 33' 40.6" W), specimens 203, 204 and 205; Saladas Centro (28[degrees] 14' 20.3" S; 58[degrees] 37' 40.4" W), specimens 128 and 129; Saladas Sur (28[degrees] 17' 37.5" S; 58[degrees] 41' 19.2" W), specimen 134; San Alonso (28[degrees] 17' 76" S; 57[degrees] 24' 45" W), specimens 186, 187, 188 and 190; Estancia San Luis (28[degrees] 6' 43.7" S; 58[degrees] 51' 48.1" W), specimens 236/ 26484, 237/26485, 238/26486 and 239/26487; Goya (29[degrees] 11' 17.2" S ; 59[degrees] 12' 36.7" W), specimens 181 to 184; San Roque (28[degrees] 41' S; 58[degrees] 42' W), specimens 135 to 137; Chavarria (28[degrees] 58' S; 58[degrees] 35' W), specimens 149 to 153; Curuzu Laurel (27[degrees] 55' 24.4" S; 57[degrees] 29' 23.5" W), specimens 220 to 222; Loreto (27[degrees] 44' 43.7" S ; 57[degrees] 14' 35.2" W), specimens 156, 223/26479 and 224; Contreras Cue (28[degrees] 5' 28.6" S ; 56[degrees] 33' 53.7" W), specimens 199, 207, 208, 210 and 211; Mbarigui (27[degrees] 33' S; 57[degrees] 31' W), specimen 174; San Miguel (28[degrees] 0' 58.6" S; 57[degrees] 36' 19.2" W), specimens 214/26478, 216 and 217; Paraje Caiman (28[degrees] 3' 3.1" S ; 57[degrees] 40' 38.4" W), specimens 225, 226/26480, 227/26481 to 228/26482, and Paraje Sarandicito (30[degrees] 14' 43.1" S; 59[degrees] 33' 46.1" W), specimens 212/26476 and 213/26477.

[FIGURE 1 OMITTED]

Chromosome preparations

Metaphase preparations were obtained from bone marrow following Ford and Hamerton (1956) and stained with Giemsa. Chromosomes were classified according to Levan et al. (1964) and FNs were computed considering autosomes and sexual chromosomes. For each specimen a minimum of 20 metaphases was analyzed. For each specimen a karyogram was considered reliable when at least five different metaphases yielded the same assembly. Chromosomes were classified into three groups: sexual chromosomes (see Results), and biarmed and telocentric autosomes. Chromosomes were joined in pairs according with their morphology and size, in decreasing order.

RESULTS

In Table 1 we present a summary of the karyomorphs of the Ctenomys Corrientes group published in the literature. In the present paper, we described a total of 15 karyomorphs. The sexual chromosome system for the Corrientes group is XX/XY; both sexual chromosomes were biarmed, as was characterized by Ortells et al. (1990). The identification of sexual chromosomes was based on the differences between males and females from each population, as well as contrasting our karyomorphs with previously reported ones (Ortells et al., 1990). In each karyomorph the sexual pair was included in a third group apart from the classification of biarmed and telocentric chromosome pairs (Figs. 2-6).

Estancia San Luis

The four individuals, two females (236 and 237) and two males (238 and 239) sampled at estancia San Luis were homozygous 2n = 48 and FN = 80 (Fig. 2a). The autosomal complement comprises 15 biarmed and 8 telocentric pairs. On the 7th biarmed pair, a secondary constriction was observed. The X chromosome is a large metacentric, while the Y chromosome is a medium-sized submetacentric. The karyomorph found in Estancia San Luis is indistinguishable from that found in Costa Mansion, Ctenomys roigi's type locality (Ortells et al., 1990), less than 10 km from Estancia San Luis.

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Mbarigui

The chromosome complement of a female (174) from Mbarigui, the type locality of Ctenomys dorbignyi was 2n = 70 FN = 84, confirming the characteristic karyotype of this species, which possesses the highest diploid number of the genus (Fig. 2b). The autosomal complement consists of 6 biarmed and 28 telocentric pairs. The 14th monobrachial pair presents a secondary constriction. This karyomorph shows the same morphology and chromosome number as the one described by Ortells et al. (1990), corresponding to the same locality. We identified the X chromosome as a large metacentric, also in accordance with Ortells et al. (1990).

Paraje Sarandicito

A male (213) and a female (212) captured at the locality of Paraje Sarandicito had a 2n=70 FN=84 karyomorph (Fig. 2c) distinguishable from the one found in Mbarigui (Fig. 2b) for having a submetacentric second pair instead of metacentric, in agreement with Arguelles et al. (2001). The Y chromosome is a medium-sized submetacentric, in agreement with previous descriptions (Ortells et al., 1990; Arguelles et al., 2001).

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

[FIGURE 6 OMITTED]

Chavarria

Specimens sampled in Chavarria depicted the same karyomorph. Three males (149, 150 and 153) and two females (151 and 152) shared a karyomorph 2n = 56 and FN = 84 (Fig. 3a). The autosomal complement of the 2n = 56 FN = 84 comprises 13 biarmed and 14 telocentric pairs, while the sexual pair consists of a mediumsized metacentric X chromosome and a small submetacentric Y chromosome. A secondary constriction was found in the 8th biarmed pair. For the same locality, Gimenez et al. (2002) and Lanzone et al. (2007) mentioned a karyomorph 2n = 58 FN = 84. However, these publications did not include any photographic material to corroborate chromosome number.

San Roque

Two females (135 and 136) and one male (137) from San Roque were analyzed. The 3 specimens had a karyomorph 2n = 62 and FN = 84, consisting of 11 biarmed and 30 telocentric autosomal pairs (Fig. 3b). A secondary constriction was observed in the 5th biarmed pair. The X chromosome is a medium- sized submetacentric, while the Y chromosome is a medium-sized metacentric. This karyomorph matches the one described for the same population by Ortells et al. (1990).

Saladas Centro

The two females (128 and 129) sampled in the locality of Saladas Centro had 2n = 54 FN = 84. A total of 14 biarmed and 12 telocentric pairs compose the autosomal complement (Fig. 4a). The 9th biarmed pair bears a secondary constriction, and the X chromosome is a large metacentric, in correspondence with an identical karyomorph found in this population by Ortells et al. (1990). These authors found two additional karyomorphs 2n = 55 and 2n = 56, both with FN = 84, which correspond to heterozygous and homozygous morphs originated by a centric fusion/fission event comprising the 7th biarmed pair.

Saladas Sur

Saladas Sur is a previously undescribed locality placed 7.3 km far from Saladas Centro in southwest direction. The karyomorph of a female (134) was 2n = 51 FN = 84 constituting a new 2n record for the Corrientes group (Fig. 4b). The autosomal complement consists of 15 biarmed pairs plus one biarmed chromosome in heterozygosis, and 8 telocentric pairs plus two telocentric chromosomes in heterozygosis. One of the chromosomes of the biarmed pairs--probably the 4th--was "orphan" and could be involved in a fusion/fission event with two telocentric chromosomes. This Robertsonian rearrangement should be confirmed by banding techniques. The X chromosome is a large metacentric, identified in comparison with the karyomorph found in the neighboring population of Saladas Centro. The 11th biarmed pair bears a secondary constriction.

Goya

The chromosome complement of the 2 females (183 and 184) and 2 males (181 and 182) sampled in Goya, the type locality of C. perrensi, was 2n = 50 FN = 84, in accordance with the karyotype previously published (Ortells et al., 1990). This karyomorph comprises 8 telocentric and 16 biarmed autosomal pairs (Fig. 4c). A secondary constriction was observed in the 9th biarmed pair. The X chromosome is a large metacentric while the Y chromosome is a medium-sized submetacentric.

Paraje Caiman

In the population sampled at Paraje Caiman, from a total of 4 specimens, 2 females (225 and 228) were heterozygous with 2n = 45 (Fig. 5b) while a female (226) and a male (227) had 2n=46 (Fig. 5a), all of which had FN = 78. In the morph with 2n = 46 the autosomal complement consists of 15 biarmed and 7 telocentric pairs. The sexual pair is heteromorphic; the X chromosome is a large submetacentric, whereas the Y chromosome is a small submetacentric. The 6th biarmed pair, a medium-sized submetacentric, bears a secondary constriction. In the 2n = 45 morph, the 3rd biarmed and the first two major telocentric chromosomes resulted "orphans", being probably involved in a fusion/fission event that originated the heterozygous condition. The 2n = 44, FN = 78 morph was not found in this population, likely due to insufficient sampling. However, the occurrence of this karyomorph is highly probable in this population, and it would be indistinguishable from the one found in San Alonso (Fig. 5c). In a previous article Gimenez et al. (2002) stated that in Paraje Caiman, in addition to the 2n = 46, a 2n = 47 morph was found. But, like in the case of Chavarria, these karyomorphs cannot be compared because there is no photographic material available.

San Alonso

San Alonso is a sandy patch located in the central area of the Provincial Reserve Esteros del Ibera. It is an island surrounded by shallow marshes that could eventually reconnect with the mainland. Two males (186 and 188) and two females (187 and 190) sampled in San Alonso had 2n = 44 and FN = 78, previously undescribed karyomorph for the Corrientes group. The autosomal complement consisted of 16 biarmed and 5 telocentric pairs, with a secondary constriction observed in the 7th biarmed pair (Fig. 5c). The sexual pair was heteromorphic, including a large submetacentric X chromosome and a small submetacentric Y chromosome.

San Miguel

The sample from San Miguel consisted of two males (214 and 217) and one female (216), with a 2n = 44 and FN = 76 karyomorph (Fig. 6a). In this case, the autosomal complement presented 15 biarmed and 6 telocentric pairs. Within the telocentric group, the two major pairs resemble the ones found in Paraje Caiman. The sexual pair was heteromorphic, including a large submetacentric X chromosome and a small submetacentric Y chromosome. This karyomorph was already published by Gimenez et al. (2002) as well as by Lanzone et al. (2007) for this locality but again lacking photographic support.

Contreras Cue

A total of 5 specimens were sampled at Contreras Cue. Four of the individuals, two females (207 and 208) and two males (210 and 211) had 2n = 42 and FN = 76 (Fig. 6b) while a female (199) was heterozygous with 2n = 41 and the same fundamental number (Fig. 6c). The autosomal complement of the 2n = 42 karyomorph consists of 16 biarmed and 4 telocentric pairs. The sexual pair is submetacentric: the X is a large chromosome, while the Y is small. The female with 2n = 41 had one extra small metacentric chromosome, and lacked two telocentric chromosomes of the autosomal complement. When compared with the karyomorph 2n = 42, these differences are most probably due to a centric fusion.

Curuzu Laurel

Two females (220 and 221) and a male (222) captured at the locality of Curuzu Laurel were homozygous with 2n = 42 and FN = 76, in agreement with the karyomorph published by Ortells et al. (1990) corresponding to the same locality. This karyomorph is indistinguishable from the 2n = 42 described for Contreras Cue (Fig. 6b).

Loreto

A total of three tuco-tucos were captured in Loreto, two males (156 and 224) and a female (223) that were homozygous with a karyomorph that was identical to the 2n = 42 found in Contreras Cue (Fig. 6b). The 2n and FN found in this locality coincide with the ones previously published by Gimenez and collaborators (2002).

Estancia La Tacuarita

Cytogenetic analyses were carried out for three individuals sampled at Estancia La Tacuarita, two females (203 and 204) and a male (205), The karyomorph was homozygous and indistinguishable from the other 2n = 42 described in this paper (Fig. 6b), and also reported by Gimenez et al. (2002) although without photographic support.

DISCUSSION

In the present work we characterized 3 new karyomorphs: 2n = 44 FN = 78 from San Alonso (Fig. 5c) plus two heterozygous 2n = 51 FN = 84 from Saladas Sur (Fig. 4b) and 2n = 45 FN = 78 from Paraje Caiman (Fig. 5c). We also showed another 5 karyomorphs from which only 2n and FN numbers have been published but without photographs depicting the morphology and size of the chromosomes: those from Chavarria (Fig. 3a), Paraje Caiman (Fig. 5a), San Miguel (Fig. 6a), Contreras Cue (Fig. 6b and c), Loreto (see Results) and estancia La Tacuarita (see Results). We also reanalyzed the previously described karyomorphs, confirming those from Mbarigui, the type locality of C. dorbignyi (Fig. 2b), Paraje Sarandicito (Fig. 2c), Goya, the type locality of C. perrensi (Fig. 4c), San Roque (Fig. 3b), Saladas Centro (Fig. 4a) and Curuzu Laurel (see Results). The finding of a new population of C. roigi (Estancia San Luis) is important because this is a critically endangered species (Bidau et al., 2008).

New chromosomal data from the Corrientes group confirm that FNs 76, 78, 80 and 84 characterize the karyomorphs of the group. Fundamental numbers 76 and 78 were found in the Ibera subgroup; FN = 80 was only found in the karyomorph from Estancia San Luis (which is indistinguishable from that of Costa Mansion, the type locality of C. roigi) and FN = 84 was found in the remainders.

The karyomorphs of the Ibera subgroup that share FN = 76 are very similar (see Results) with 2n = 41, 42 and 44. The same occurs with those that share FN = 78 that depict 2n = 44, 45 and 46. Differences in 2n without changes in FN might be mainly explained by Robertsoninan events, although banding techniques are required to confirm it and to identify the chromosomes involved. Since within each FN, 2n range is limited, the rearrangements involved might be easy to track by G-banding techniques. The karyomorphs that share FN = 84, on the contrary, include a broader range of chromosomal numbers, from 2n = 56 to 2n = 70. In these cases, although Robertsonian changes are also probably the most frequent rearrangement, as those described by Lanzone et al. (2002) and Lanzone et al. (2007), the relationships among the karyomorphs might be more difficult to establish. The ample range of chromosomal numbers suggests a more complex scenario that may include parallelisms, reversions and/or convergences.

New chromosomal data shown in this paper broaden the chromosomal information of the Ctenomys Corrientes group, essential to understand the role of chromosomal variability in speciation and hybridization processes. However, phylogeny (Caraballo et al., 2012), population genetics (Gomez- Fernandez et al. 2012), morphology and ecology should also be taken into account to establish species boundaries in this interesting group of tuco-tucos.

Recibido 2 diciembre 2014. Aceptado 21 abril 2015. Editor asociado: E Palma

ACKNOWLEDGEMENTS

This work was supported by grants from the Agencia Nacional de Investigaciones Cientificas y Tecnicas (PICT 3836/1) and Consejo Nacional de Investigaciones Cientificas y Tecnicas (PIP 5776 and PIP 2012-2014) from Argentina. Authors thank Drs. Lidia Poggio and Liliana Maria Mola from the Laboratorio de Citogenetica y Evolucion, Departamento de Ecologia Genetica y Evolucion. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, and also Rodrigo Alvarez, Pablo Belluscio, Maria Jimena Gomez Fernandez, Marcelo Kittlein, Fernando Mapelli, Patricia Mirol, Matias Mora, Vanina Raimondi, Veronica Trucco Cano, and Laura Wolfenson for assistance at the field work. We also like to thank Diana Avedikian, Veronica Romero, Cecilia Kopuchian and Sergio Rodriguez Gil, two anonymous reviewers whose comments have improved the manuscript, and the editor for his suggestions.

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Diego A. Caraballo (1), Paola C. Jablonski (2), Pablo J. Rebagliati (2), and Maria Susana Rossi (1)

(1) IFIBYNE-CONICET. Laboratorio de Fisiologia y Biologia Molecular, Dep. Fisiologia, Biologia Molecular y Celular. Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires, Ciudad Universitaria, Pabellon II, 2do piso, EHA1428, Buenos Aires, Argentina. Tel. +54 11 4576 3386/68. [Correspondence: Maria Susana Rossi <srossi@fbmc.fcen.uba.ar>]

(2) Laboratorio de Citogenetica y Evolucion, Departamento de Ecologia Genetica y Evolucion, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellon II, 2do piso, EHA1428, Buenos Aires, Argentina.
Table 1
Karyomorphs of the Ctenomys Corrientes group. 1: Ortells et al.
(1990), 2: Arguelles et al. (2001), 3: Gimenez et al. (2002) and
4: Lanzone et al. (2007).

Locality               2n/FN values                  Giemsa-stained
                       (Published in)                  karyomorph
                                                     (Published in)

Costa Mansion          48/80 (1, 3, 4)               1
Estancia San Luis      48/80 (this paper)            This paper
Colonia Brougnes       48/80 (3)                     --
Estancia Rosarito      51-52/80 (4)                  --
Mbarigui               70/84 (1, 2, 3, 4,            1, this paper
                       this paper)
Paraje Angostura       70/84 (4)                     --
Paraje Sarandicito     70/84 (2, 3, this paper)      2, this paper
San Roque              62/84 (1, 3, this paper)      1, this paper
MF Mantilla            62/84 (1)                     1
Santa Rosa             65-66/84 (3, 4)               --
Chavarria              56/84 (this paper),           This paper, --
                       58/84 (3, 4)
Saladas Centro         54/84 (this paper), 55-56/    This paper, 1
                       84 (1, 3, 4)
Saladas Sur            51/84 (this paper)            This paper
Ruta Saladas-          54-58/84 (3)                  --
  Mburucuya Km 10-12
Ruta Saladas-          54-56-58/84 (1, 3)            1
  Mburucuya Km 7
Goya                   50/84 (1, 2, this paper)      1, this paper
Colonia 3 de abril     50/84 (2)                     --
Rincon de Ambrosio     50/84 (2)                     --
Pago Alegre            56/84 (3, 4)                  --
Mburucuya              58/84 (1)                     1
Pago de los            56/84 (4)                     --
  Deseos-Km 10
Yatayti-calle          53-54/84 (1)                  1
Paraje Santo           54-55/82 (4)                  --
  Domingo
San Alonso             44/78 (this paper)            This paper
Paraje Caiman          45-46/78 (this paper)         This paper
                       46-47/78 (3)
San Miguel             44/76 (3, 4, this paper)      This paper
Contreras Cue          41-42/76 (3, this paper)      This paper
Estancia La            42/76 (3, this paper)         This paper
  Tacuarita
Curuzu Laurel          42/76 (1, 3, 4, this paper)   1, this paper
Loreto                 42/76 (3, this paper)         This paper
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Title Annotation:texto en ingles
Author:Caraballo, Diego A.; Jablonski, Paola C.; Rebagliati, Pablo J.; Rossi, Maria Susana
Publication:Mastozoologia Neotropical
Date:Dec 1, 2015
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