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13
Chromosomal Changes and Adaptation
Of Cichlid Fishes During Evolution
Eliana Feldberg1, Jorge Ivan Rebelo Porto1and
Luis Antonio Carlos Bertollo2
1
Department of Aquatic Biology, National Institute for
Research in the Amazon (INPA), Brazil.
2
Department of Genetic and Evolution, Federal University of São Carlos, Brazil
e-mail: [email protected]
INTRODUCTION
Why have cichlids awakened the interest of so many people throughout
the world? Two words probably answer this question: aesthetics and
behavior. The astounding number of fish hobbyists increases everyday,
mainly because cichlids are so distinctive in appearance. This ornamental
fish group represents 2% of total exported from Brazil (Ferreira,
1981; Leite and Zuanon, 1991). In addition, it also plays a very important
role in fisheries either as a food source for population or as a recreation / commercially
important activity for ecotourists termed "catch and release fishing".
Belonging to the order Perciformes, cichlids occupy the fourth place among
fishes concerning the number of species, encompassing nearly 227 genera
and 1,292 species distributed throughout South, (287 sp), North, and
Central America, (89 sp), Africa (900), Madagascar (13) and India (3sp)
(Kullander, 1998). They are now recognised as a monophyletic group
(Kaufman and Liem, 1982), which stands out by its evolutionary success,
that is, its high speciation rate and specialisation among fish. Cichlids can
to adapt to extreme environmental conditions, even though they prefer lentic
environments (Lowe-McConnell, 1969; Liem, 1974; Kornfield, 1978;
Kornfield et al., 1979; Thompson, 1979; see also Chippari-Gomes et al.,
this volume). Perhaps their species richness and diversity in trophic adaptations are directly related to this wide exploitation of habitats and
niches.
Phylogenetic analyses of morphological and molecular characters
have contributed to our understanding of the evolutionary history of the
Feldberg, Eliana, J. I. R. Porto, and L. A. C. Bertollo. 2003. Chromosomal changes and
adaptation of cichlid fishes during evolution. In: A.L. Val and B.G. Kapoor (eds.), Fish
Adaptation. Science Publishers, Inc, Enfield – NH, USA. pp. 285-308
286
cichlids. Some uncertainties, such as their origin as well as their monophiletic /
polyphiletic nature, have become better understood trough phylogenetic
reconstructions. In this chapter, we present an overview of the cytogenetic
studies on cichlids, inferring the main chromosomal rearrangements and
pathways that probably occurred in their evolutionary process, taking
into account some recent phylogenetic propositions. For database of fish
chromosome, the reader is referred to Klinkhardt et al. (1995).
CHROMOSOME NUMBERS
Perciformes is the most species-abundant order among the Teleostei. Freshwater is the main habitat of just 14% of these species. Of the 150 families
of Perciformes, the karyotype of representatives of only 50 families has
been analysed, i.e., 420 species, which show the following distribution:
283 (67%) with 2n=48 chromosomes, 124 (30%) with 2n < 48 and 13 (3%)
with 2n > 48 (Brum, 1995). The chromosomal number taken as the ancestral
diploid number for this fish order is 2n=48 acrocentric chromosomes
(Brum, 1995).
Until 1979, the haploid / diploid number of just a few cichlid species
(about 60) had been determined. Thompson (1979), at that time, described
the karyotypes of 42 Neotropical cichlid species and provided the first
scenario for understanding the karyoevolutionary pathways in this family. Later, Kornfield (1984) presented additional information for the chromosomes of 70 species. Subsequently, this number increased significantly
and the karyotype of 135 species of cichlids has been determined (Table
13.1), 106 from the New World (33 genera) and 29 from the Old (11
genera). However, these data are still very poor if we consider the number
of known species in this fish family. Furthermore, many of these studies
report only the haploid / diploid number and chromosomal arms (Table
13.1).
As expected for a perciform fish, the standard karyotype of 48
monoarmed chromosomes is found more often among the cichlids. Although the diploid chromosome number ranges from 2n=32 to 2n=60
chromosomes, more than 60% of the species present a karyotype with
2n = 48. A bimodal distribution of diploid numbers is evident and related
to the geographic distribution of the species; African cichlids have a
modal diploid number of 2n = 44, with a variation from 32 to 48 chromosomes, and FN (fundamental number) 44 to 88, while Neotropical cichlids
have a modal diploid number of 2n= 48, with a variation from 38 to 60
chromosomes and FN = 44 to 118 (Table 13.1, Figure 13.1).
From a cytogenetic viewpoint, cichlids have been considered a conservative group because of the standard macrokaryotype (Thompson,
1979; Kornfield, 1984; Feldberg and Bertollo, 1985a). Even today, with a
much larger number of analysed species, the trend for maintaining the
287
Table 13.1 Chromosomal characterisation of the Cichlidae family. n = haploid number; 2n = diploid number; KF = karyotypic formulae;
FN = fundamental number; NOR = nucleolus organizer region; m, sm = metacentric, submetacentric; st,a = subtelocentric, acrocentric;
* = updated species names as shown in the Fish Database http:// www.fishbase.org/search.cfm.
Subfamily
Etroplinae
Species
Etroplus maculatus
Locality
Etroplus suratensis
Pseudocrenilabrinae
Haplochromis burtoni*
Haplochromis flaviijosephi1*
Hemichromis bimaculatus
Hemichromis bimaculatus
Melanochromis auratus
Neolamprologus leleupi*
Oreochromis macrochir*
Oreochromis macrochir*
Oreochromis alcalicus *
Oreochromis andersonii
Oreochromis andersonii*
Oreochromis aureus*
Oreochromis aureus*
Oreochromis mossambicus*
2n KF
46
FN
48
África
Sea of Galilee
África
Zaire
Sea of Galilee
Oreochromis mossambicus*
40
44
44
44
46
48
44
44
48
44
44
44
44
44
44
Oreochromis niloticus*
Oreochromis niloticus
Oreochromis niloticus*
Pelvicachromis pulcher*
n
22 44
aquaculture
22 44
40
48
14m,sm+26st,a
10m,sm+34st,a
54
54
12m,sm+34st,a
88
58
6m,sm+38st,a
50
4m,sm+40st,a
6m,sm+38st,a
10m,sm+34st,a
6m,sm+38st,a
44m,sm
48
50
54
50
88
NOR
Reference
Natarajan and Subrahmanyam,
1974
Natarajan and Subrahmanyam,
1974
Thompson, 1981
Kornfield et al., 1979
Post, 1965
Zahner, 1977
Thompson, 1981
Post, 1965
Jalabert et al., 1971
Vervoort, 1980
Post, 1965
Vervoort, 1980
Vervoort, 1980
Thompson, 1981
Natarajam and Subrahmanyam,
1968
Prasad and Manna, 1976;
Fukuoka and Muramoto, 1975
Chervinski, 1964; Jalabert et al,
1971; Arai and Koike, 1980;
Foresti et al, 1993
Majumdar and McAndrew,1986
Badr and El Dib, 1976
Post, 1965
288
Table 13.1 (Contd.)
Subfamily
Species
Pseudocrenilabrus multicolor*
Sarotherodon galilaeus
Sarotherodon galilaeus*
Sarotherodon mossambica
Sarotherodon multifasciatus
Tilapia busumana
Tilapia congica
Tilapia guineensis
Tilapia macrocephala
Tilapia mariae
Tilapia mariae
Tilapia rendalli
Tilapia rendalli
Tilapia sparrmanii
Tilapia sparrmanii
Tilapia zillii
Tilapia zillii
Tristramella sacra
Tristramella simonis
?
Gen. n. Sp. n.
Cichlinae
Cichla sp.
Cichla sp.
Cichla monoculus
Cichla temensis
Cichla temensis
Locality
África
Zaire
África
Ribeirão Preto,SP
R. Iguaçu, Brasil
Zaire
África
Sea of Galilee
Sea of Galilee
Sea of Galilee
n
2n KF
44
44
FN
44
44
44
44
44
44
32
40
40
44
44
6m,sm+38st,a
6m,sm+38st,a
50
50
10m,sm+34st,a
8m,sm+36st,a
54
52
4m,sm+36st,a
8m,sm+32st,a
16m,sm+28st,a
10m,sm+34st,a
44
48
60
54
42
42
38
44
44
44
8m,sm+34st,a
8m,sm+34st,a
50
50
10m,sm+34st,a
6m,sm+38st,a
6m,sm+38st,a
54
50
50
Reference
Post, 1965
Badr and El Dib, 1976, 1977;
Vervoort, 1980
Thompson, 1981
Nijjhae et al., 1983
Nijjhae et al.,1983
Vervoort, 1980
Vervoort, 1980
Jakowska, 1950
Vervoort, 1980
Thompson, 1981
Michele and Takahashi, 1977
Mizoguchi and Martins-Santos,
1999
Vervoort, 1980
Thompson, 1981
Badr and El Dib, 1977
48
Martins-Santos et al., 1992
44
Tucuruí, PA
Amazonas, AM
Amazonas, AM
Commercial source
Amazonas, AM
48
48
48
48
48
48st,a
48st,a
48st,a
48st,a
48st,a
NOR
2 cr.
48
48
48
48
48
2 cr.
2 cr.
2 cr.
2 cr.
Venere, 1988
Alves, 1998
Alves, 1998
Thompson, 1979
Alves, 1998
289
Table 13.1 (Contd.)
Subfamily
Species
Crenicichla sp.
Crenicichla “sexatilis”
Crenicichla cf. saxatilis
Crenicichla iguassuensis
Crenicichla lacustris
Crenicichla lepidota
Crenicichla lucius
Crenicichla niederleinii
Crenicichla niederleinii
Crenicichla notophthalmus
Crenicichla reticulata
Crenicichla semifasciata
Crenicichla semifasciata*
Crenicichla sp.
Locality
R Paraná, Argentina
Uruguai
R. Peixe-boi, PA
R. Iguaçu, PR
Registro, SP
Crenicichla sp.
Crenicichla spA.
Crenicichla spB.
R Paraguai, MT
Amazonas, AM
Amazonas, AM
Miranda, MS
Commercial Source
R. Paraná, PR
Misiones, Argentina
Commercial source
R.Paraná, PR
Misiones, Argentina
Commercial source
R. Uatumã, AM
Misiones, Argentina
Miranda, MS
R Paraná, Argentina
n
2n
48
24 48
48
48
24 48
24
48
48
48
48
48
48
48
48
48
48
24 48
48
KF
6m,sm+42st,t
4m,sm+44st,a
FN
54
52
NOR
2 cr.
8m,sm+40st,a
6m,sm+42st,a
56
54
6m,sm+42st,a
6m,sm+42st,t
6m,sm+42st,a
54
54
54
2 cr.
14m,sm+34st,a
62
2 cr.
6m,sm+42st,a
6m,sm+42st,a
54
54
2 cr.
6m,sm+42st,a
6m,sm+42st,a
54
54
2 cr.
2 cr.
46
48 6m,sm+42st,a
48 8m,sm+40st,a
54
56
2 cr.
2 cr.
2 cr.
2 cr.
2 cr.
4 cr.
Reference
Roncati et al., 1996
Oyhenart-Perera et al., 1975
Farias et al., 1999b
Mizoguchi et al., 2000
Feldberg and Bertollo, 1985a,b
Scheel, 1973
Thompson, 1979
Martins et al., 1995
Roncati et al, 2000
Thompson, 1979
Thompson, 1979
Alves et al., 1999
Fenocchio et al., 1994;Roncati
et al., 1996
Rezende et al., 1996
Salgado et al., 1994
290
Table 13.1 (Contd.)
Subfamily
Astronotinae
Geophaginae
Species
Crenicichla strigata
Crenicichla vittata
Locality
Commercial source
Miranda, MS
Astronotus crassipinnis
Astronotus ocellatus
Amazonas, AM
Astronotus sp.
Chaetobranchopsis australis
Miranda, MS
Manaus, AM
R Paraguai, MT
Miranda, MS
Acarichthys heckelii
Apistogramma agassizii
Apistogramma agassizii
Apistogramma borellii
Apistogramma borellii
Apistogramma borellii*
Apistogramma cacatuoides
Apistogramma ortmanni
Apistogramma ortmanni
Apistogramma pertensis
Apistogramma steindachneri*
Commercial source
Commercial source
n
2n KF
48 6m,sm+42st,a
24 48 6m,sm+42st,a
FN
54
54
NOR
48 18m,sm+30st,a
48
48 6m,sm+42st,a
66
96
54
2 cr.
Krychanã et al. , 1996
Zahner, 1977
Thompson, 1979
Scheel, 1973
24 48 12m,sm+36st,a
24 48 12m,sm+36st,a
48
24 48 48st,a
60
60
2 cr.
2 cr.
48
1cr.
48 6m,sm+42st,t
46 24m,sm+22st,a
54
70
38 22m,sm+16st,a
46 24m,sm+22st,a
60
46
86
70
46
92
Commercial source
2 cr.
24
20
23
Commercial source
23
23
Commercial source
19
24
Reference
Thompson, 1979
Thompson, 1979
Thompson, 1979
Scheel, 1973
Scheel, 1973
Thompson, 1979
Scheel, 1973
Scheel, 1973
Thompson, 1979
Scheel, 1973
Post, 1965
Zahner, 1977
291
Table 13.1 (Contd.)
Subfamily
Species
Apistogramma trifasciata
Dicrossus filamentosus*
Dicrossus maculatus
Geophagus altifrons
Geophagus brasiliensis
Locality
Misiones, Argentina
Commercial source
Brotas, SP
São Carlos, SP
Pirassununga, SP
Registro, SP
Commercial source
L Rodrigo de Freitas, RJ
48 6m,sm+42st,a
48
48
48
Maricá, RJ
Araquá, Tietê,SP
R Claro,Tietê, SP
Hortelã,Paranapanema,S
P
Jacutinga,
Paranapanema, SP
Pirapo, Paranapanema
R Sapucaí, MG
Rio Iguaçu, PR
48 8m,sm+40st,a
48 8m,sm+40st,a
48 4m,sm+44st,a
Rio Iguaçu, PR
48 6m,sm+42st,a
n
2n KF
46
46 12m,sm+34st,a
FN
NOR
48 4m,sm+44st,a
48 3m,sm+45st,a
48
52
51
9092
50
50
50
50
52
56
2 cr.
54
2 cr.
2 cr.
2 cr.
2 cr.
Feldberg and Bertollo, 1985 a, b
Thompson, 1979
Oliveira et al., 1994; Brum
et al., 1998
Brum et al. 1998
Corazza et al., 1998
2 cr.
56
56
52
2 cr.
2 cr.
2 cr.
54
2 cr.
Couto, et al., 1998
Mizoguchi and Martins-Santos,
2000
Quijada and Cestari, 1998
58
23
Amazonas, AM
Ribeirão Preto, SP
24
24
24
24
48
48
48
48
48
48
2m,sm+46st,a
2m,sm+46st,a
2m,sm+46st,a
2m,sm+46st,a
4m,sm+44st,a
8m,sm+40st,a
48
2 cr.
2 cr.
2 cr.
2 cr.
2 cr.
Reference
Thompson, 1979
Scheel, 1973
Michele and Takahasi, 1977
Zahner, 1977
292
Table 13.1 (Contd.)
Subfamily
Species
Geophagus sp.
Geophagus surinamensis
Geophagus surinamensis
Guianacara sp.
Gymnogeophagus gymnogenys
Gymnogeophagus balzanii
Locality
R. Paraná, Argentina
Amazonas, AM
Commercial source
R Trombetas, PA
Jacui/Tramandaí, RS
Miranda, MS
Gymnogeophagus balzanii
Gymnogeophagus labiatus
Gymnogeophagus lacustris
Gymnogeophagus rhabdotus
Gymnogeophagus sp. n.
Mikrogeophagus ramirezi
Mikrogeophagus ramirezi*
Satanoperca acuticeps
Satanoperca jurupari
Satanoperca jurupari
Rio Peixe-boi, PA
Marchantaria and
Catalão, AM
Catalão, AM
n
2n
48
24 48
48
48
48
24- 48
26
48
48
48
48
48
24
24
48
48
KF
NOR
4m,sm+44st,a
4m,sm+44st,a
4m,sm+44st.a
4m,sm+44st,a
2m,sm+46st,a
FN
50
52
52
52
52
50
4 cr.
4 cr.
Reference
Roncati et al. 1996
Thompson, 1979
Feldberg et al., 1990
Peixoto and Erdtmann, 1988
Feldberg and Bertollo, 1984;
1985b
Scheel, 1973
Post, 1965
2m,sm+46st,a
4m,sm+44st,a
4m,sm+44st,a
4m,sm+44st,a
50
52
52
52
2 cr.
2 cr.
4 cr.
Mendonça et al., 1999
2 cr.
2 cr.
2 cr.
64
6m,sm+42st,a
54
48 4m,sm+44st,a
5m,sm+43st,a
6m,sm+42st,a
52
53
54
293
Table 13.1 (Contd.)
Subfamily
Cichlasomatinae
Species
Satanoperca jurupari*
Satanoperca jurupari*
Satanoperca pappaterra
Locality
Commercial source
Amazônia
Rio Paraná
Acaronia nassa
Marchantaria and
Catalão, AM
Aequidens metae
Aequidens plagiozonatus
Aequidens pulcher
Aequidens sp.
Aequidens tetramerus
Amphilophus citrinellus*
Amphilophus macracanthus*
Archocentrus centrarchus*
Archocentrus nigrofasciatus*
Archocentrus septemfasciatus*
Archocentrus spilurus*
Bujurquina sp
Bujurquina vittata
n
R Paraná, PR
2n KF
48 4m,sm+44st,a
48
48 6m,sm+42st,a
FN
52
NOR
54
2 cr.
Reference
Thompson, 1979
Moreira Filho, et al., 1980
50 50st,a
50
2 cr.
48 6m,sm+42st,a
48
54
24
Amazônia
Rio Peixe-boi, PA
48 48st,a
48
24
48 36m,sm+12st,a
48
48 8m,sm+40st,a
2 cr.
82
48
82
84
96
56
24
24
48
48 6m,sm+42st,a
48 6m,sm+42st,a
24
48
48 4m,sm+44st,a
48 6m,sm+42st,a
R Cuarto, Costa Rica
96
54
54
96
96
52
54
24
I. Mindú, AM
Misiones, Argentina
48 8m,sm+40st,a
44
56
2 cr.
2 cr.
Thompson, 1979
Martins-Santos et al., 1990
Scheel, 1973
Scheel, 1973
Nishikawa et al., 1973
Zahner, 1977
Thompson, 1979
Hinegardner and Rosen, 1972
Scheel, 1973
Zahner, 1977
Thompson, 1979
Thompson, 1979
Scheel, 1973
Zahner, 1977
Thompson, 1979
Thompson, 1979
Scheel, 1973
Mendonça (Pers. Comml)
294
Table 13.1 (Contd.)
Subfamily
Species
Bujurquina vittata*
Caquetaia kraussii*
Caquetaia spectabilis
Cichlasoma amazonarum
Cichlasoma beani
Cichlasoma bimaculatum
Cichlasoma bimaculatum
Cichlasoma dimerus
Cichlasoma facetum
Cichlasoma facetum
Cichlasoma facetum
Cichlasoma facetum
Cichlasoma octofasciatus
Cichlasoma octofasciatus
Cichlasoma paranaense
Locality
2n
44
50
Amazonas, Brasil
50
I. Mindú, AM
48
Mexico
48
44
48
Misiones, Argentina
48
Uruguai
24 48
Registro, SP
24 48
Rio Claro, SP
24 48
S Cachoeira, São Mateus
48
do Sul, PR
48
48
Guaravera, Londrina, PR
48
Cichlasoma paranaense
Cichlasoma portalegrense*
Cichlasoma salvini
Rio Paraná, PR
Cichlasoma salvini
Cichlasoma sp. A
Cichlasoma sp. C
Cichlasoma trimaculatus
Cleithracara maronii*
Cleithracara maronii*
Herichthys cyanoguttatus*
Herichthys cyanoguttatus*
Belize
n
KF
26m,sm+18st,a
6m,sm+44st,a
50st,a
2m,sm+46st,a
6m,sm+42st,a
44st,a
6m,sm+42st,a
FN
70
56
50
50
54
44
54
8m,sm+40st,a
10m,sm+38st,a
10m,sm+38st,a
10m,sm+38st,a
56
58
58
58
6m,sm+42st,a
14m,sm+34st,a
96
54
62
48 20m,sm+28st,a
52
68
82
104
52 28m,sm+24st,a
80
24
24
R Paraguai, MT
46
48 6m,sm+42st,a
24
Mexico
50
48
48 6m,sm+42st,a
54
82
100
94
54
NOR
2 cr.
2 cr.
2 cr.
Reference
Thompson, 1979
Thompson, 1979
Thompson, 1979
Santos et al., 1998
Thompson, 1979
Oyhenart-Perera et al., 1975
Quijada and Cestari, 1998
6cr.
Zahner, 1977
Thompson, 1979
Loureiro and Dias, 1998
5cr.
3 cr.
2 cr.
Scheel, 1973
Zahner, 1977
Thompson, 1979
Scheel, 1973
Thompson, 1979
Scheel, 1973
Zahner, 1977
Zahner, 1977
Thompson, 1979
295
Table 13.1 (Contd.)
Subfamily
Species
Herichthys labridens
Herichthys minckleyi*
Heros severus*
Heros sp
Heros sp
Heros sp
Herotilapia multispinosa
Herotilapia multispinosa
Hypselecara coryphaenoides*
Laetacara curviceps
Laetacara curviceps*
Mesonauta festivus
Mesonauta festivus*
Mesonauta festivus*
Mesonauta festivus*
Mesonauta insignis
Nandopsis tetracanthus*
Nannacara anomala
Nannacara anomala
Nannacara anomala
Neetroplus nematopus
Parachromis dovii
Parachromis managuensis*
Parachromis managuensis*
Locality
S. Rioverde, Mexico
Mexico
n
2n KF
48 6m,sm+42st,a
48 6m,sm+42st,a
FN
54
54
NOR
48 6m,sm+42st,a
54
2 cr.
48
48 6m,sm+42st,a
48 6m,sm+42st,a
96
54
54
48 12m,sm+36st,a
60
48
48 8m,sm+40st,a
48 12m,sm+36st,a
48 6m,sm+42st,a
96
56
60
54
44
48
48
48
48
62
56
56
96
54
24
24
24
Marchantaria and
Catalão, AM
Commercial source
19
19
Médio R. Negro
4 cr.
24
Baixo e Médio R. Negro
Re San Juan, Cuba
24
22
18m,sm+26st,a
8m,sm+40st,a
8m,sm+40st,a
6m,sm+42st,a
4 cr.
Reference
Thompson, 1979
Thompson, 1979
Post, 1965: Scheel, 1973
Post, 1965
Scheel, 1973
Zahner, 1977
Thompson, 1979
Thompson, 1979
Scheel, 1973
Scheel, 1973
Santos et al., 2001
Scheel, 1973
Zahner, 1977
Thompson, 1979
Santos et al., 2001
Ráb et al., 1983
Post, 1965
Scheel, 1973
Thompson, 1979
Thompson, 1979
Thompson, 1979
Zahner, 1977
Thompson, 1979
296
Table 13.1 (Contd.)
Subfamily
Species
Pterophyllum scalare*
Pterophyllum scalare
Locality
Symphysodon aequifasciatus
Commercial source
Amazônia, Brasil
Symphysodon discus
Symphysodon discus
Manacapuru, AM
Amazônia, Brasil
Amazônia, Brasil
Uaru amphiacanthoides
n 2n KF
24
24
48 4m,sm+44st,a
48 4m,sm+44st,a
60 44m,sm+16st, a
30
R.Amazonas, Tefé
Amazônia, Brasil
60 58m,sm+2st,a
60 44m,sm+16micr.
60 42m,sm+18 micr
citótipos: A e B
60 42m,sm+18micr
60 42m,sm+18micr
60 48m,sm+12micr
46m,sm+14micr
46 8m,sm+38st,a
FN
52
52
104
116
118
104
102
102
102
108
106
54
NOR
2 cr.
5cr.
5 cr.
2 cr.
2 cr.
Reference
Post, 1965
Scheel, 1973
Thompson, 1979
Krychanã et al., 1996
Ohno and Atkin, 1966
Scheel, 1973
Thompson, 1979
Salgado et al., 1996b
Mesquita et al., 2000
Salgado et al., 1996a
Thompson, 1979
297
Fig. 13.1 Frequency distribution of diploid chromosome number of cichlids from Old and
New world cichlids.
diploid number of 2n=48 chromosomes, mainly acrocentric ones, is still
apparent. Nevertheless, even though the diploid number remains 48 chromosomes for 60% of the cichlids, we believe that the term “conservative”
chromosomal evolution is not appropriate for describing the real condition of this fish group. Indeed, despite the predominance of 2n = 48
acrocentric chromosomes, the occurrence of several chromosomal
rearrangements is very clear, as can be seen through the FN variation.
PATTERN OF CHROMOSOMAL CHANGES
Chromosomal data remain an important tool for evolutionary analyses of
fish, now improved by the development of the molecular cytogenetics, despite the explosive use of molecular genetics analyses on ichthyological
studies these last years. Species diagnosis, polymorphism detection and
physical chromosome mapping are some of the fields enriched by use of
modern cytogenetic methods. However, some difficulties inherent to fish
chromosomes offer some limitations to cytogenetic analysis of this group,
such as their overall small size and low resolution for multiple chromosomal banding (i.e., G-banding), current techniques used in analyses of
specialised vertebrates studies. Nevertheless, understanding the evolutionary trends and pathways, as well as the correlated chromosomal
rearrangements in cichlids, has been improved the study of their
chromosomes.
298
A chromosome based phylogenetic tree for the cichlids is not yet possible,
since the characters suitable for this purpose are few and not all species
have a complete set of karyotypic data. However, the two most recent
phylogenetic trees based on molecular and morphological characters, make
possible the inference of some patterns of chromosomal evolution that
have occurred within this family. Kullander (1998) proposed a new
phylogenetic hypothesis for the Cichlidae family based on 91 morphological characters from 43 South American and 7 Old World terminal
taxa, and organised it into the following subfamilies: Etroplinae,
Pseudocrenilabrinae, Retroculinae, Cichlinae (Tribes: Crenicichlini and
Cichlini), Heterochromidinae, Astronotinae (Tribes: Astronotini and
Chaetobranchini), Geophaginae (Tribes: Geophagini, Acarichthyini and
Crenicaratini) and Cichlasomatinae (Tribes: Acaroniini, Cichlasomatini
and Heroini). In this tree, Etroplinae (Malagasy / Indian cichlids) and
Pseudocrenilabrinae (African cichlids) are sister groups and comprise the
sister groups of all cichlids (including the heterochromidin Heterochromis,
an African genus, within the Neotropical clade).
Farias et al. (2000a) presented a phylogenetic analysis for the cichlids that
combines mitochondrial (16S rRNA) and nuclear DNA (TMO-M27, TMO4C4) with morphological characters (from Kullander, 1998). They suggest that
the subfamilie Etroplinae (Malagasy / Indian cichlids) is the most basal
lineage for family Cichlidae and that Heterochromidinae and
Pseudocrenilabrinae (African clade) is the sister group of the remaining
subfamilies that form the Neotropical clade. These trees are shown in
Figure 13.2, with the diploid numbers included on the major groups.
However, due to lack of terminal taxa, it is only possible to infer the
chromosome rearrangements at the main lineages level.
Fig. 13.2 Chromosomal numbers on phylogenetic trees of cichlids (adapted from Farias et
al., 2000a) produced by morphological and total evidence (16S + Nuclear loci + morphological data).
299
According to Thompson (1979), the ancestral karyotype of cichlids is
represented by 2n=48 acrocentrics (monoarmed chromosomes) and so
any difference from this condition would represent a derivative evolutionary state. The chromosomal variation on the Etroplinae is 46 to 48 and for
the Pseudocrenilabrinae clade 32 to 48 chromosomes. Considering that
2n=48 acrocentrics represents the ancestral diploid number for the family, it may be suggested that the chromosomal evolution in the two most
basal clades occurred in two directions: maintenance of the diploid number
2n=48 and decrease of this number (probably through chromosomal
fusions since the presence of bi-armed chromosomes is evident in several
species). Unfortunately, the number of analysed cichlid species of the
Old World is small even though the region harbours more than twothirds of the 1,292 species of the family described to date. Compared to
the Neotropics, Old World cichlids present less karyotypical variation,
both diploid number and chromosomal structure (Table 13.1). In the African lineage, Tilapia-Sarotherodon presents a very long pair of
subtelocentric that represents a marker chromosome for this lineage
(Kornfield et al., 1979).
On the other hand, the chromosomal variation in New World cichlids is
more pronounced, with the diploid number ranging from 38 to 60 chromosomes, evidenced in the derived lineages Cichlasomatinae and
Geophaginae. Based on these data, we suggest three evolutionary directions in this clade. The first direction is characterised by the maintenance
of 2n = 48 acrocentrics, or with a few metacentric-submetacentric chromosomes, due mainly to pericentric inversions. This evolutionary trend
is present in species of the subfamilies Cichlinae, Astronotinae, Geophaginae
and Cichlasomatinae. The second evolutionary trend includes a decrease
in diploid number in parallel with a larger number of bi-armed chromosomes (M-SM), suggesting chromosomal fusions and pericentric inversions. This direction is shown in subfamilies Cichlinae (genus Crenicichla:
1 species), Geophaginae (genera Apistogramma: 9 species; Dicrossus: 2 species) and Cichlasomatinae (genera Bujurquina: 1 species; Cichlasoma: 2
species; Laetacara: 1 species; Nannacara: 1 species and Uaru: 1 species).
The third direction results from an increase in diploid number (2n = 50
and 52), although most of the chromosomes remain acrocentric, suggesting a derived character. It is possible that its ancestor already presented
2n=48, with some M-SM chromosomes due to pericentric inversions,
and now subsequent centric fissions explain the diploid number increase. This
evolutionary direction is present only in species of subfamily
Cichlasomatinae (Acaronia nassa, Caquetaia spectabilis, C. kraussii, Cichlasoma
salvini, and Cleithracara maronii). In this last subfamily, genus Symphysodon
should be specifically analysed because additional data is required before we can understand its main evolutionary trend. This genus, with
300
only two reported species, possesses an uncommon karyotype in respect
to both Neotropical cichlids and the entire group of Perciformes, in which
a diploid number >48 was found in only 13 species. The two Symphysodon
species presented 2n=60 chromosomes, mainly of the M-SM type, one
species with single NORs and the other with multiple NORs, different
cytotypes and large blocks of constitutive heterochromatin (Salgado et al.,
1994, 1995, 1996b; Mesquita et al. 2000).
Thompson (1976) and Kornfield (1984) suggest that Symphysodon
might have a relationship between high chromosome number and DNA
amount (1.5 pg for S. aequifasciatus) since this kind of karyotype was
derived through several stages, among which polyploidisation could have
taken place. However, the c DNA value for Neotropical cichlids (2n=48)
reported by Hinegardner and Rosen (1972) is 2.4 pg on average, which
suggests, contrarily, that there is no reason a priori to assume that
Symphysodon had experienced events of polyploidisation. Up to now, the
few examples of polyploidisation in Neotropical fishes seem to be restricted to silurifoms (callichthiids and loricariids), as pointed out by
Oliveira et al. (1988).
Given the proposed phylogenetic trees, for family Cichlidae (Kullander,
1998, Farias et al., 2000a), the chromosomal data corroborate the basal
position of genus Cichla, which presents 2n=48 acrocentric chromosomes
in three species. Although genera Astronotus and Crenicichla are also basal
in the phylogeny of Kullander (1998), these genera present M-SM
chromosomes, considered a derived character in cichlids
(Thompson, 1979), indicating the occurrence of some rearrangements,
such as pericentric inversions. Thus, this fact corroborates the molecular
data that place Crenicichla on a more derived position. However, its
proximity with genus Apistogramma should be analysed, since the latter
presents a great karyotypic diversity, including species with a diploid
number lower than 48, indicating other rearrangements in addition to
inversions, such as chromosome fusions. In contrast, genus Crenicichla
presents certain karyotype homogeneity among the 15 species analysed,
with the first pair of chromosomes very characteristic, usually seen as a big
metacentric / submetacentric with a conspicuous interstitial secondary
constriction. This pair of chromosome is also found in genera Geophagus
(except Geophagus brasiliensis) and Gymnogeophagus. These two genera also
present non-Robertsonian rearrangements (pericentric inversions type) and
stable karyotypes, with a great similarity to Crenicichla. However,
Geophagus brasiliensis is thought to be a “species complex” (Kullander,
1998; Farias et al., 2000a). Indeed, chromosomal data corroborate this
complexity, since a variation from 2 to 8 M-SM chromosomes occurs for
specimens from different collection sites, an indication of the existence of
cryptic species in this group (Brum et al.,1998) or, alternatively,
301
chromosomal races in an early speciation process. Concerning
Chaetobranchopsis, its karyotype with 2n=48 acrocentrics also corroborates
the position as a basal clade among the Geophagines, according to the
Farias et al. (2000a) phylogenetic tree.
Kullander and Ferreira (1988) distinguished genus Satanoperca from
genus Geophagus. Chromosomal data support this separation since the
two Satanoperca species analysed present a more derived karyotype in
relation to genus Geophagus. Satanoperca species also do not present the
characteristic pair of chromosomes observed in Geophagus, except for S.
pappaterra. According to Mendonça et al. (1999), three cytotypes were
evidenced in S. jurupari, relative to the number of M-SM chromosomes
(4, 5, 6), which could represent another case of two chromosomal races,
showing 4 and 6 M-SM respectively, and possibly a hybrid, with 5 M-SM
chromosomes.
CHROMOSOMAL BANDING
Despite recent advance achieved in fish cytogenetics through high–resolution molecular techniques, chromosomal banding in cichlids is restricted
to visualisation of the nucleolus organising regions (NORs) and
heterochromatin (C-banding). The few exceptions are the use of restriction
enzimes and FISH in Oreochromis niloticus (Oliveira and Wright, 1998;
Oliveira et al., 1999).
Family Cichlidae may be characterised as a fish group presenting a
single NOR system (only one pair of NORs) located on the larger
chromosome of the complement (Table 13.1). Indeed, there are exceptions.
This feature appears to be a plesiomorphic character state for cichlids
(Feldberg and Bertollo, 1985b). Hsu et al. (1975) suggested that species
presenting a single pair of NORs may be considered more primitive in
terms of rDNA distribution in the karyotype than those with multiple
NORs. Chromosomal rearrangements, such as translocation and inversion,
transpose repeated sequences of these sites to other chromosomes, thus
characterising multiple NORs as a derived character state. This seems
true for some cichlid species in which multiple NOR systems occur as
well as a shift of the NORs from the first chromosomal pair to other
chromosomes of the complement.
Even considering the low number of cichlids analysed for this character
(45 species, Table 13.1), the available data allow drawing the following
trend: the only two African cichlids analysed for NORs presented single
NORs (Kornfield et al., 1979; Mizoguchi and Martins-Santos, 1999). In the
Neotropical clade, all analysed species of the Astronotinae subfamily show
a single NOR, located on the first chromosome pair of the complement
(Feldberg and Bertollo, 1985b; Krichanã et al., 1996). In Cichlinae, of the
16 species analysed, only one (a single population of Crenicichla lepidota)
302
presented multiple NORs (Martins et al., 1995). Among Geophaginae, of
9 species, only Satanoperca jurupari and S. acuticeps presented multiple
NORs, these located on ST-A chromosomes of medium size (Salgado et
al., 1994; Mendonça et al., 1999; Farias et al., 2000b). Among
Cichlasomatinae, of 15 species, 5 present multiple NORs, i.e., Caquetaia
spectabilis (Salgado et al., 1995), Cichlasoma paranaense from one population (Loureiro and Dias, 1998), Mesonauta insignis and M. festivus (Santos
et al., 2001), and Symphysodon aequifasciatus (Salgado et al, 1995; Mesquita
et al., 2000).
The number of Cichlidae species analysed for constitutive heterochromatin is also reduced, a fact that impairs useful comparative analysis.
Reports on C-banding for Old World cichlids includes those for Sarotherodon
(Kornfield et al., 1979), Oreochromis (Kornfield et al., 1979; Majumdar and
McAndrew, 1986; Oliveira and Wright, 1998) and Tilapia (Kornfield et al.,
1979), showing that blocks of heterochromatin seem to be restricted in
and around the centromere in all species analysed thus far, although the
short arms of a few chromosomes are totally heterochromatic. The large
first chromosome pair that occurs in these fish species also seems to be a
good chromosome marker since large heterochromatic blocks are observed.
Thirty-two species were analysed for C-banding among the New World
cichlids, all showing constitutive heterochromatin mainly on the
pericentromeric region of the chromosomes (Feldberg et al., 1990; MartinsSantos et al., 1990; Martins et al.,1995; Krichanã et al., 1996; Roncati et al.,
1996; 2000; Salgado et al., 1996b; Alves, 1998; Loureiro and Dias, 1998;
Alves et al., 1999; Farias et al., 1999b; 2000b; Mendonça et al. 1999; Mesquita
et al., 2000; Santos et al., 2001). Interspecific differences relative to interstitial heterochromatic blocks were also observed. Short arms of
subtelocentric chromosomes were totally heterochromatic, as were the
NOR sites for some species.
C-bands emerge as an important cytogenetic marker for Neotropical
cichlid species, even among those closely related. For example, the three
species of the genus Cichla, have identical karyotype macrostructure but
C-band differences are observed (Alves, 1998). Large amounts of
constitutive heterochromatin were also observed in two genera of
Cichlasomatinae, Symphysodon and Pterophylum (Mesquita et al., 2000;
Nascimento et al., 2001).
HYBRIDISATION
Hybridisation may be considered an outer source of genetic variation
for populations, providing sufficient genetic variation for organisms
adapting to new environments (Futuyma, 1993). Hybrids tend to present
inter-mediate characters between the parental species and may exceed
them in vigor (Hubbs, 1955).
303
Several cases of hybridisation have been reported among cichlid fishes.
Lowe-McConnell (1958), reporting the occurrence of hybrid tilapias in
some lakes of the Old World, suggested that this hybridisation resulted
from intentional introduction of new species of Tilapia from other lakes.
Although viable hybrids have already been produced both from interand intra-generic breeding, e.g., Tilapia x Oreochromis and Cichlasoma
nigrofasciatum x C. cyanoguttatum, a large difference in the sex ratio was
found among the descendents (Kornfield, 1984). McElroy and Kornfield
(1993) also verified the presence of a hybrid between two African cichlid
species, Pseudotropheus zebra and Labeotropheus fuelleborni, somewhat distinct in morphology concerning the parents, yet with a greater similarity
to P. zebra.
Sawaya and Maranhão (1946), studying the reproductive behaviour of
genus Cichla in captivity, reported a hybridisation case between C. temensis
and C. ocellaris. However, the latter species probably refers to C. monoculus
since C. ocellaris does not occur in the Brazilian Amazonia (Kullander,
personal comm.). Alves (1998) observed that Cichla sp. presents intermediate characteristics, both at the morphological and karyotypic levels,
between C. monoculus and C. temensis. She suggested that the ancestor of
the Cichla sp. could be the result of an interspecific crossing between
these two species. Indeed, C. monoculus, C. temensis and the Cichla sp. are
syntopic species in several places of the Amazonian basin. Andrade et al.
(2001), sequencing the 16S rRNA gene in 40 Cichla specimens, confirmed
the hybridisation between C. monoculus and C. temensis in all sites where
the two species occur in simpatry.
CONCLUSION
A general overview of the karyoevolution of cichlids has been presented.
Although the variation of diploid number ranges from 2n = 32 to 2n = 60,
a variation of 2n = 46-48 for Malagasy / Indian cichlids, 2n=44 for African and 2n = 48 for Neotropical ones has been established. In cichlids,
chromosomal rearrangements are postulated based only on standard chromosomal characterisation (Giemsa, NORs and C-bands) since the use of
high resolution chromosome banding is still limited among cichlids. This
tentative cytotegenetic framework was possible only by comparisons with
available phylogenetic hypothesis. The available chromosomal data support the hypothesis of Farias et al. (1999a) that Neotropical cichlids, due
to their karyotypic diversity, show a higher rate of evolution than observed
among the cichlids from Old World.
Acknowledgements
This work was suported by INPA and CNPq.
304
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