Genetica 119: 11–17, 2003.
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
11
Inter and intra-specific hybridization in tuco-tucos (Ctenomys)
from Brazilian coastal plains (Rodentia: Ctenomyidae)
Adriana Gava & Thales R.O. Freitas
Departamento de Genética, Universidade Federal do Rio Grande do Sul, Porto Alegre, P.O. Box 15053, 91501-970,
Rio Grande do Sul, Brazil (Fax: +55-014-33167311; E-mail: [email protected])
Received 15 May 2002 Accepted 22 October 2002
Key words: chromosomes, colonization history, Ctenomys minutus, hybrid zone, rodent, selection, subterranean
Abstract
The present work describes chromosomal polymorphisms in zones of contact between divergent populations
of Ctenomys minutus parapatrically distributed in the coastal plain of southern Brazil, and inter-specific
hybridization with C. lami a closely related species. A sample of 171 specimens from 32 sample sites distributed along 161 km of the coastal plain was cytogenetically analyzed. Nine polymorphic populations were
found: four with specimens with 2n = 46–48 (autosomal arm number (AN) = 76); three only have specimens with 2n = 47 and 48; one population sampled presented specimens with 2n = 43–46 (AN = 74–76)
and one population with 2n = 50–52 (AN = 76–80). The remainder populations were fixed for 2n = 42, 46
or 48. The variation is the result of Robertsonian mechanisms of chromosomal evolution and a fusion in
tandem rearrangement. The polymorphisms have been considered the result of secondary contact of populations after divergence in allopatry. The geomorphological evolution of the coastal plain provides clues
to the possible existence of past geographic barriers acting over populations of Ctenomys, during the
Holocene.
Introduction
The subterranean rodents of the genus Ctenomys comprise more than 50 species endemic to the Patagonian
subregion of the neotropics (Reig et al., 1990). They
arose in the early Pleistocene and underwent explosive diversification probably as a response to climatic
changes (Reig et al., 1990; Lessa & Cook, 1998;
Cook, Lessa & Hadley, 2000). The genus is strikingly variable regarding diploid numbers, 2n = 10–70
(Novello & Lessa, 1986; Anderson, Yates & Cook,
1987; Cook, Anderson & Yates, 1990; Reig et al.,
1992; Garcia et al., 2000a,b), C-banding patterns
(Vidal-Rioja, 1985; Gallardo, 1991; Massarini et al.,
1991; Reig et al., 1992; Freitas, 1994; Massarini,
Dyzenchauz & Tiranti, 1998; Garcia et al., 2000a)
and satellite copy numbers – RPCS (Rossi, Reig &
Zorzopulos, 1990, 1993; Rossi et al., 1995; Novello
et al., 1996; Slamovits et al., 2001). Four species do occur in southern Brazil: C. flamarioni,
C. lami, C. minutus and C. torquatus. Their distribution, taxonomic status, ecology, population genetics,
craniometric and cytogenetical attributes, and spermatozoa morphology were previously addressed (Freitas
& Lessa, 1984; Moreira et al., 1991; Freitas, 1994,
1995a,b, 1997, 2001; Gastal, 1994a,b; Marinho &
Freitas, 2000).
Ctenomys minutus inhabits the sandy fields and
dunes of coastal plains of the southern Brazilian states
of Santa Catarina and Rio Grande do Sul (Freitas,
1995a). A cytogenetic survey revealed the existence
of an impressive karyotypic variation never recorded
before for a species of tuco-tuco. At least seven karyotypes exist: 2n = 46a, 46b and 47–50 (autosomal arm
number (AN) = 76) and 2n = 42 (AN = 74). Taking
the 2n = 50 karyotype as a standard, nine chromosomic arms are involved with the observed variation.
The 20/17 and 23/19 fusions are present in all karyotypes while a tandem fusion between arms 16 and 24
occurs only in the 2n = 42 and 46b karyotypes. Arm
12
Figure 1. Map showing trapping sites of C. minutus populations fixed for diploid numbers 2n = 42, 46 or 48, and polymorphic populations
from intra-specific and inter-specific contact zones as displayed by the legend: (a) populations fixed for 2n = 46 (white circles), 2n = 48 (black
circles), polymorphic populations from contact zones between 2n = 46 × 48 (stars) and 2n = 48 of C. minutus and 2n = 56 of C. lami (triangle);
(b) populations fixed for 2n = 48 (black circles), for 2n = 42 (circles with pattern), and polymorphic populations from the contact zone between
2n = 42 × 48 (gray circle).
22 is fused to the new chromosome in the latter
karyotype. The metacentric chromosome number 2 is
dissociated in two arms in the 2n = 48 karyotype. The
same holds for 2n = 46b, but its 2p arm suffered an
inversion – 2pinv (Freitas, 1997).
Each karyotype can be assigned to a particular
geographic area with divergent populations separated
by geographic barriers or having contiguous distributions. The populations with 2n = 46a are widely
distributed over 135 linear km from the southern banks
of Araranguá River to the east of Barros Lake, having
a contiguous distribution with the southern populations with 2n = 48 (Figure 1). West of Barros Lake
the existence of polymorphic populations was recorded, characterizing a hybrid zone (Freitas, 1997;
Gava & Freitas, 2002). The southernmost record of
populations fixed for 2n = 48 was at Palmares do
Sul, 30 km apart from the hybrid zone, while the
2n = 42 and 46b were recorded 120 and 150 km to
the south in Mostardas and Tavares localities, respectively. With the exception of the 2n = 50 karyotype,
which is distributed in a northern area (Jaguaruna
Beach, Santa Catarina state) and separated from the
2n = 46a populations by the Araranguá River, the
other karyotypes have separate but contiguous distributions devoid of any obvious physical barriers
between them. Populations of C. lami have diploid numbers varying from 2n = 54–58 and occupy
an elevated area at western Barros Lake (Freitas,
1995a).
The main goal of this paper is to report zones
of contact between the cytotypes 2n = 46 × 48 and
42 × 48 of C. minutus (Nehring, 1887), and interspecific hybridization among C. minutus and C. lami
(Freitas, 2001), a recently described species (Freitas,
2001).
13
Table 1. Sample localities of 171 specimens of Ctenomys minutus. (LN = locality number, N = sample size, 2n/NA = diploid
number and autosomal arm numbers, and P = frequency of
karyotypes)
Locality
South Caieira Lake
South Traı́ras Lake
Northeast Barros Lake
Northeast Barros Lake
East Barros Lake
LN
1
2
3
4
N
3
5
6
6
5
6
East Barros Lake
Estância dos Weber
North Emboaba Lake
Marechal Osório Park
South Barros Lake
6
7
8
9
10
6
7
5
12
7
West Barros Lake 1
West Barros Lake 2
West Barros Lake 3
11
12
13
6
6
6
Passinhos
East Passo do Paulo
Estância Velha
East Manuel Nunes Lake
Pitangueira
Rincão da Fortaleza
14
15
16
17
18
19
4
4
4
6
6
6
Fortaleza Lake
20
5
South Fortaleza Lake
21
10
South Suzana Lake
22
4
Palmares do Sul
km 35 Capivari-Tavares Road
km 53 Capivari-Tavares Road
km 64 Capivari-Tavares Road
km 96 Capivari-Tavares Road
km 101 Capivari-Tavares Road
km 108 Capivari-Tavares Road
23
24
25
26
27
28
29
8
4
5
3
4
3
6
2n/AN
P
46/76
46/76
46/76
46/76
47/76
48/76
47/76
48/76
48/76
46/76
46/76
46/76
47/76
48/76
48/76
48/76
50/76
51/76
51/77
51/78
51/80
52/79
48/76
48/76
46/76
46/76
48/76
46/76
47/76
48/76
46/76
47/76
48/76
47/76
48/76
46/76
47/76
48/76
48/76
48/76
48/76
48/76
48/76
48/76
43/74
44/74
45/75
46/76
1.0
1.0
1.0
0.5
0.167
0.333
0.333
0.667
1.0
1.0
1.0
1.0
0.143
0.857
1.0
1.0
0.167
0.167
0.167
0.167
0.167
0.167
1.0
1.0
1.0
1.0
1.0
0.167
0.333
0.5
0.2
0.4
0.4
0.4
0.6
0.25
0.5
0.25
1.0
1.0
1.0
1.0
1.0
1.0
0.166
0.166
0.5
0.166
Table 1. (continued)
km 115 Capivari-Tavares Road
km 120 Capivari-Tavares Road
km 125 Capivari-Tavares Road
Total
30
31
32
3
3
2
42/74
42/74
42/74
1.0
1.0
1.0
171
Material and methods
The 171 specimens (83 females and 88 males)
of Ctenomys were collected from 32 sample sites
between east Barros Lake and south Mostardas locality in the coastal plain of Rio Grande do Sul, Brazil
(Table 1; Figure 1). Skulls and skins were deposited
in the collection of the Departamento de Genética,
Universidade Federal do Rio Grande do Sul. Mitotic
preparations were obtained according to the technique
of Ford and Hamerton (1956), and the diploid numbers were determined after analyses of 10 metaphases
stained with Giemsa. G-banding analyses of two animals per karyotype were performed according to the
procedures of Seabright (1971).
Results
Seven polymorphic sites were sampled in the zone of
contact between the cytotypes 2n = 46 and 48 (sites
4, 5, 10 and 19–22) localized east of Barros Lake to
the western–southwestern margin of Fortaleza Lake
(Table 1; Figure 1(a)). If the maximum observed
distributional limits of polymorphic populations is
considered, variation of C. minutus metacentric chromosome frequency occurs in a 10 km-wide-zone. The
hybrid zone between the populations with 2n = 42 and
48 occurs at km 108 of Capivari-Tavares Road, where
one polymorphic population was sampled (site 29;
Table 1; Figure 1(b)). An additional polymorphic site
(13) was found in western Barros Lake, near an area
of distribution of another tuco-tuco species, C. lami
(Table 1; Figure 1(a)).
The hybrid zone between the karyotypes with
2n = 46 and 48 was thoroughly sampled – 132 specimens (61 females and 71 males) with three different
diploid numbers, 2n = 46–48 (AN = 76 – Table 1; Figure 1(a)). These karyotypes were described by Freitas
(1997), and the zone analyzed in detail regarding its
characteristics, origin and formation (Gava & Freitas,
2002). Seven polymorphic populations were found:
14
four with individuals with 2n = 46–48 (AN = 76),
while the others have only specimens with 2n = 47 and
48. Individuals with heteromorphic karyotypes consist
of 37.8% of the total number of specimens from polymorphic sites. Northeast to southeast of Barros Lake,
eight monomorphic sites with 2n = 46 were recorded
(sites 1–3, 7–9, 16 and 17) while south and southwest
Barros Lake six monomorphic sites with 2n = 48 were
recorded (sites 6, 11, 12, 14, 18 and 19 – Table 1;
Figure 1(a)).
South Palmares do Sul, five sites (sites 24–28),
with 19 specimens have a typical 2n = 48 karyotype
(AN = 76 – Figure 1(b)). The southernmost record of
the karyotype was at km 101 of the Capivari-Tavares
Road (site 28). Seven km further, a polymorphic population with specimens with four karyotypes 2n =
43–46 (AN = 74/75/76, site 29) was recorded (Table 1;
Figures 1(b), 2(a) and (b)). The remaining sample sites
were fixed with 2n = 42 (AN = 74, sites 30–32).
Figure 3. Karyotype of Ctenomys from a contact zone between C.
minutus with 2n = 48 and C. lami with 2n = 56: (a) G-banded karyotype of a female with 2n = 51 and AN = 78. The heteromorphic
pair number one from an individual with 2n = 52 is in prominence
(b).
West Barros Lake (site 13) three diploid numbers,
2n = 50–52, all with different AN (ANs = 76/77/78/79
and 80) were recorded in a sample of six specimens
(Table 1 – Figures 1(a) and 3). Pairs 1 and 2 of
the 2n = 48 karyotype are clearly involved in the observed polymorphisms. Third and fourth unidentified
chromosomes also are involved in the polymorphisms.
Discussion
Figure 2. Karyotypes of C. minutus: (a) standard stained karyotype
from a male with 2n = 43, AN = 74; (b) its G-banded karyotype.
The heteromorphic pair number one from an individual with 2n = 45
is in small box.
The karyotypic diversity of C. minutus was generated by Robertsonian rearrangements and tandem
fusions involving nine chromosomes, taking the karyotype with 2n = 50 as a standard (Freitas, 1997). The
populations with 2n = 48 are interacting with populations which have different degrees of divergence.
The difference between the karyotypes with 2n = 46
and 48 is a Robertsonian rearrangement, while in the
2n = 42, chromosomes differ by a tandem fusion of
two acrocentrics, plus a Robertsonian fusion that created a new readily distinguishable large chromosome.
The other difference is a metacentric chromosome in
the 2n = 42 that is dissociated in the karyotype with
2n = 48.
A commonplace result of this divergence, in the
absence of selection against hybrids in both cases, is
a difference in the degree of introgression among the
populations. In the contact zone among populations
with 2n = 42 and 48 an array of intermediate karyo-
15
types will be generated, and parental-like karyotypes
will be formed in a smaller proportion than in the
other contact zone. Halfway between km 101 and
115 of Capivari-Tavares Road, the southern and northern records of the karyotypes with 2n = 48 and 42,
respectively, three specimens have the expected 2ns
and ANs if they were the F1 progenie of individuals with 2n = 42 and 48. The other karyotypes are
putative backcrosses: the 2n = 44 and 46 are homokaryotypes, while one specimen with 2n = 43 has one
metacentric chromosome in heterozygosis (Figure 2).
No parental-like karyotypes were found.
The hybrid zone between the 2n = 46 and 48 is
located near a lowland area: the Cidreiras’ Swamp
which may represent a barrier preventing C. minutus
colonization and dispersion. Some hybrid zones tend
to rest in regions of low population density, which may
act as a barrier obstructing or diminishing gene flow
(Barton & Hewitt, 1985; Hewitt, 1988). Despite the
narrowness of the chromosomal hybrid zone (10 km),
intense gene flow might exist among the karyotypes,
because parental-like individuals must actually be the
result of mixed ancestry.
The recently described species C. lami occupies
a sandy, elevated area which spreads out from east
Guaiba River toward northwest Barros Lake (Freitas,
1995a). It is bounded at northeast by Pachecos’
Swamp and southeast by Touros’ Swamp. Populations with 2n = 48 were recorded in a elevated area
in the southwest banks of Barros Lake, but in sample
site 13, a polymorphic population was recorded. All
of the west side of Barros Lake is a marshy lowland zone occupied by rice plantation, the area that
can be used by Ctenomys populations following the
lake bank being no more than 1 km wide. Reig,
Contreras and Piantanida (1966) collected a specimen at Santo Antonio da Patrulha, northeast Barros Lake (Freitas, personal communication) identified
as C. minutus. Freitas (1997, 2001) considered the
2n = 50 a missed determination, as it corresponds to
the populations of C. minutus from Araranguá locality. Another possibility is that the specimen actually
corresponds to a hybrid like the specimens recently
sampled.
Hybrid zone origins and role of chromosome
variation
The limited area of contact between the populations
with 2n = 46 and 48 occurs west of Barros Lake and
is likely to be a product of secondary contact after
divergence in allopatry (Gava & Freitas, 2002). The
cytotypes have large distributions, the 2n = 46 over
135 km from the southern banks of Araranguá River
to Emboaba Lake (Freitas, 1997) and the cytotype
2n = 48 extends south for almost 110 linear km. A
parapatric model of divergence is feasible in this case,
but there is no reason to think that the new chromosome would spread to a new area and not to the
range of the primitive karyotype, unless the rearrangement is strongly underdominant. However, the lack
of evidence for heterozygote deficiency or excess in
polymorphic populations of C. minutus as weak selection gradient, supported by a clinal analysis, suggests
that the rearrangement is not underdominant and that
the cline is not maintained by a selection gradient
due to an environmental ecotone (Gava & Freitas,
2002). Therefore clinal patterns of variation observed
herein may be the result of near neutral dispersal of
animals and time since secondary contact (Endler,
1977).
The stasipatric model (White, 1978) could be used
to explain the divergence of the 2n = 42, which populations have a discrete distribution, but the lack of
evidence for strong underdominance of hybrids does
not support this hypothesis. Furthermore, geological
data concerning the formation of the coastal plain suggests the existence in the past of a drainage system that
certainly had acted as a geographic barrier (Corrêa,
1996).
According to Steinberg and Patton (2000), allopatry is the geographic context of speciation in subterrranean rodents. The geographic distribution of C.
minutus populations strictly follows the coastal line
and is limited at west by the Geral Mountains as well
by the Patos Lagoon. Such linear pattern of distribution constrains the possible areas of contact between
divergent populations and may account for narrowness of the zones. This may be explained by a series
of characteristics, including the fragmented nature
of occupation of the habitat by populations, which
delay a further contact between parental populations.
Such characteristic is a common feature among subterranean rodents and may be responsible, jointly with
low vagility, small population density, high population
turn over, selection against hybrids and recent time of
secondary contact, for the narrowness of the hybrid
zones (Gastal, 1994a; Busch et al., 2000; Steinberg &
Patton, 2000).
Chromosomal variation has been considered the
main factor associated with speciation in the genus
Ctenomys. This claim is mostly based on gross
16
morphology of banded karyotypes, their distribution,
and a widespread notion that chromosomal variation
in Ctenomys is species-specific. However, as these
studies have begun to encompass a greater number
of populations over the species ranges, chromosomal
polytypism as well as polymorphism are becoming
common features of the genus. It have been reported for C. conoveri (Anderson, Yates & Cook, 1987;
Ortells, Contreras & Reig, 1990; Reig et al., 1992),
C. boliviensis (Anderson, Yates & Cook, 1987), C.
magellanicus (Gallardo, 1991), C. torquatus (Freitas
& Lessa, 1984) C. pearsoni (Novello & Lessa, 1986),
C. perrensi (Garcia et al., 2000b), C. rionegrensis
(Ortells, Contreras & Reig, 1990) and C. talarum
(Reig et al., 1992).
The origin of these polymorphisms were not
addressed, however, if chromosomal rearrangements are neutral or only weakly underdominant, the conditions required for their fixation are
relaxed, but they are less likely to reduce hybrid fitness (Reiseberg, 2001). It is likely that
the described polymorphisms are neutral and may
act as transient polymorphisms in the populations.
The role of the chromosome variability as a reproductive barrier and thus as the main causative factor in speciation of the genus is still
controversial. The interactions of divergent populations in hybrid zones may be important in inputting
genetic variability into them and thus influencing
their subsequent evolution (Steinberg & Patton, 2000).
Another possibility (not exclusive) is the intense
flow of neutral genes and restrict gene flow of genomic blocks by means of suppression of recombination associated with rearrangements (Reiseberg,
2001). Present and future research concerning the genomic processes that underlie chromosomal change
(Slamovits et al., 2001) and of the genetic control
of meiosis will probably provide a framework from
which conceptual advances can be expected (Lessa,
2000).
Acknowledgements
Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq), Financiadora de Estudos e Projetos (FINEP) and Fundação de Amparo à Pesquisa
do Rio Grande do Sul (FAPERGS) have supported this study. The authors are grateful to Elise
Giacomoni, Fernanda Bitencourt, Vanina Heusser and
Tarik El Jundi for help in the field work.
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