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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 ad- aptations 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. Fresh- water 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. Al- though 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 Species Locality n 2n KF FN NOR Reference Etroplinae Etroplus maculatus 46 Natarajan and Subrahmanyam, 1974 Etroplus suratensis 48 Natarajan and Subrahmanyam, 1974

Pseudocrenilabrinae Haplochromis burtoni* África 40 14m,sm+26st,a 54 Thompson, 1981 Haplochromis flaviijosephi1* Sea of Galilee 44 10m,sm+34st,a 54 Kornfield et al., 1979 Hemichromis bimaculatus 44 Post, 1965 Hemichromis bimaculatus 44 88 Zahner, 1977 Melanochromis auratus África 46 12m,sm+34st,a 58 Thompson, 1981 Neolamprologus leleupi* 48 Post, 1965 Oreochromis macrochir* 44 Jalabert et al., 1971 Oreochromis macrochir* Zaire 44 6m,sm+38st,a 50 Vervoort, 1980 Oreochromis alcalicus * 48 Post, 1965 Oreochromis andersonii 44 4m,sm+40st,a 48 Vervoort, 1980 Oreochromis andersonii* 44 6m,sm+38st,a 50 Vervoort, 1980 Oreochromis aureus* Sea of Galilee 44 10m,sm+34st,a 54 Kornfield et al., 1979 Oreochromis aureus* 44 6m,sm+38st,a 50 Thompson, 1981 Oreochromis mossambicus* 44 44m,sm 88 Natarajam and Subrahmanyam, 1968 Oreochromis mossambicus* 44 Prasad and Manna, 1976; Fukuoka and Muramoto, 1975 Oreochromis niloticus* 22 44 Chervinski, 1964; Jalabert et al, 1971; Arai and Koike, 1980; Foresti et al, 1993 Oreochromis niloticus aquaculture 22 44 Majumdar and McAndrew,1986 Oreochromis niloticus* 40 Badr and El Dib, 1976 Pelvicachromis pulcher* 48 Post, 1965

288 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Pseudocrenilabrus multicolor* 44 Post, 1965 Sarotherodon galilaeus 44 2 cr. Badr and El Dib, 1976, 1977; Kornfield et al., 1979 Sarotherodon galilaeus* 44 6m,sm+38st,a 50 Vervoort, 1980 Sarotherodon mossambica África 44 6m,sm+38st,a 50 Thompson, 1981 Sarotherodon multifasciatus 44 Nijjhae et al., 1983 Tilapia busumana 44 Nijjhae et al.,1983 Tilapia congica Zaire 44 10m,sm+34st,a 54 Vervoort, 1980 Tilapia guineensis 44 8m,sm+36st,a 52 Vervoort, 1980 Tilapia macrocephala 32 Jakowska, 1950 Tilapia mariae 40 4m,sm+36st,a 44 Vervoort, 1980 Tilapia mariae África 40 8m,sm+32st,a 48 Thompson, 1981 Tilapia rendalli Ribeirão Preto,SP 44 16m,sm+28st,a 60 Michele and Takahashi, 1977 Tilapia rendalli R. Iguaçu, Brasil 44 10m,sm+34st,a 54 2 cr. Mizoguchi and Martins-Santos, 1999 Tilapia sparrmanii Zaire 42 8m,sm+34st,a 50 Vervoort, 1980 Tilapia sparrmanii África 42 8m,sm+34st,a 50 Thompson, 1981 Tilapia zillii 38 Badr and El Dib, 1977 Tilapia zillii Sea of Galilee 44 10m,sm+34st,a 54 Kornfield et al., 1979 Tristramella sacra Sea of Galilee 44 6m,sm+38st,a 50 Kornfield et al., 1979 Tristramella simonis Sea of Galilee 44 6m,sm+38st,a 50 Kornfield et al., 1979

? Gen. n. Sp. n. 44 48 Martins-Santos et al., 1992

Cichlinae Cichla sp. Tucuruí, PA 48 48st,a 48 Venere, 1988 Cichla sp. Amazonas, AM 48 48st,a 48 2 cr. Alves, 1998 Cichla monoculus Amazonas, AM 48 48st,a 48 2 cr. Alves, 1998 Cichla temensis Commercial source 48 48st,a 48 Thompson, 1979 Cichla temensis Amazonas, AM 48 48st,a 48 2 cr. Alves, 1998

289 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Crenicichla sp. R Paraná, Argentina 48 6m,sm+42st,t 54 2 cr. Roncati et al., 1996 Crenicichla “sexatilis” Uruguai 24 48 4m,sm+44st,a 52 Oyhenart-Perera et al., 1975 Crenicichla cf. saxatilis R. Peixe-boi, PA 48 2 cr. Farias et al., 1999b Crenicichla iguassuensis R. Iguaçu, PR 48 8m,sm+40st,a 56 2 cr. Mizoguchi et al., 2000 Crenicichla lacustris Registro, SP 24 48 6m,sm+42st,a 54 2 cr. Feldberg and Bertollo, 1985a,b Crenicichla lepidota 24 Scheel, 1973 Crenicichla lepidota Miranda, MS 48 6m,sm+42st,a 54 2 cr. Feldberg and Bertollo, 1985a,b Crenicichla lepidota Commercial Source 48 6m,sm+42st,t 54 Thompson, 1979 Crenicichla lepidota R. Paraná, PR 48 6m,sm+42st,a 54 4 cr. Martins et al., 1995 Crenicichla lepidota Misiones, Argentina 48 Roncati et al, 2000 Crenicichla lucius Commercial source 48 Thompson, 1979 Crenicichla niederleinii R.Paraná, PR 48 14m,sm+34st,a 62 2 cr. Martins et al., 1995 Crenicichla niederleinii Misiones, Argentina 48 Roncati et al., 2000 Crenicichla notophthalmus Commercial source 48 6m,sm+42st,a 54 Thompson, 1979 Crenicichla reticulata R. Uatumã, AM 48 6m,sm+42st,a 54 2 cr. Alves et al., 1999 Crenicichla semifasciata Misiones, Argentina 48 Roncati et al., 2000 Crenicichla semifasciata* Miranda, MS 24 48 6m,sm+42st,a 54 2 cr. Feldberg and Bertollo, 1985a,b Crenicichla sp. R Paraná, Argentina 48 6m,sm+42st,a 54 2 cr. Fenocchio et al., 1994;Roncati et al., 1996 Crenicichla sp. R Paraguai, MT 46 Rezende et al., 1996 Crenicichla spA. Amazonas, AM 48 6m,sm+42st,a 54 2 cr. Salgado et al., 1994 Crenicichla spB. Amazonas, AM 48 8m,sm+40st,a 56 2 cr. Salgado et al., 1994

290 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Crenicichla strigata Commercial source 48 6m,sm+42st,a 54 Thompson, 1979 Crenicichla vittata Miranda, MS 24 48 6m,sm+42st,a 54 2 cr. Feldberg and Bertollo, 1985a,b

Astronotinae Astronotus crassipinnis Amazonas, AM 48 18m,sm+30st,a 66 2 cr. Krychanã et al. , 1996 Astronotus ocellatus 48 96 Zahner, 1977 Astronotus ocellatus Commercial source 48 6m,sm+42st,a 54 Thompson, 1979 Astronotus ocellatus 24 Scheel, 1973

Astronotus ocellatus Miranda, MS 24 48 12m,sm+36st,a 60 2 cr. Feldberg and Bertollo, 1985a,b Astronotus ocellatus Manaus, AM 24 48 12m,sm+36st,a 60 2 cr. Feldberg and Bertollo, 1985a,b Astronotus sp. R Paraguai, MT 48 Rezende et al., 1996 Chaetobranchopsis australis Miranda, MS 24 48 48st,a 48 1cr. Feldberg and Bertollo, 1985a,b

Geophaginae Acarichthys heckelii Commercial source 48 6m,sm+42st,t 54 Thompson, 1979 Apistogramma agassizii Commercial source 46 24m,sm+22st,a 70 Thompson, 1979 Apistogramma agassizii 20 Scheel, 1973 Apistogramma borellii 23 Scheel, 1973 Apistogramma borellii Commercial source 38 22m,sm+16st,a 60 Thompson, 1979 Apistogramma borellii* 23 46 Scheel, 1973 Apistogramma cacatuoides 23 86 Scheel, 1973 Apistogramma ortmanni Commercial source 46 24m,sm+22st,a 70 Thompson, 1979 Apistogramma ortmanni 19 Scheel, 1973 Apistogramma pertensis 24 Post, 1965 Apistogramma steindachneri* 46 92 Zahner, 1977

291 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Apistogramma trifasciata Misiones, Argentina 46 Roncati et al., 2000 Dicrossus filamentosus* Commercial source 46 12m,sm+34st,a 58 Thompson, 1979 Dicrossus maculatus 23 Scheel, 1973 Geophagus altifrons Amazonas, AM 48 4m,sm+44st,a 52 2 cr. Salgado et al., 1995 Geophagus brasiliensis Ribeirão Preto, SP 48 3m,sm+45st,a 51 Michele and Takahasi, 1977 Geophagus brasiliensis 48 90- Zahner, 1977 92 Geophagus brasiliensis Brotas, SP 24 48 2m,sm+46st,a 50 2 cr. Feldberg and Bertollo, 1985 a, b Geophagus brasiliensis São Carlos, SP 24 48 2m,sm+46st,a 50 2 cr. Feldberg and Bertollo, 1985 a, b Geophagus brasiliensis Pirassununga, SP 24 48 2m,sm+46st,a 50 2 cr. Feldberg and Bertollo, 1985 a, b Geophagus brasiliensis Registro, SP 24 48 2m,sm+46st,a 50 2 cr. Feldberg and Bertollo, 1985 a, b Geophagus brasiliensis Commercial source 48 4m,sm+44st,a 52 Thompson, 1979 Geophagus brasiliensis L Rodrigo de Freitas, RJ 48 8m,sm+40st,a 56 2 cr. Oliveira et al., 1994; Brum et al., 1998 Geophagus brasiliensis Maricá, RJ 48 6m,sm+42st,a 54 2 cr. Brum et al. 1998 Geophagus brasiliensis Araquá, Tietê,SP 48 2 cr. Corazza et al., 1998 Geophagus brasiliensis R Claro,Tietê, SP 48 2 cr. Corazza et al., 1998 Geophagus brasiliensis Hortelã,Paranapanema,S 48 2 cr. Corazza et al., 1998 P Geophagus brasiliensis Jacutinga, 48 2 cr. Corazza et al., 1998 Paranapanema, SP Geophagus brasiliensis Pirapo, Paranapanema 48 8m,sm+40st,a 56 2 cr. Martins et al., 1995 Geophagus brasiliensis R Sapucaí, MG 48 8m,sm+40st,a 56 2 cr. Couto, et al., 1998 Geophagus brasiliensis Rio Iguaçu, PR 48 4m,sm+44st,a 52 2 cr. Mizoguchi and Martins-Santos, 2000 Geophagus brasiliensis Rio Iguaçu, PR 48 6m,sm+42st,a 54 2 cr. Quijada and Cestari, 1998

292 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Geophagus sp. R. Paraná, Argentina 48 50 Roncati et al. 1996 Geophagus surinamensis Amazonas, AM 24 48 4m,sm+44st,a 52 2 cr. Feldberg and Bertollo, 1985a,b Geophagus surinamensis Commercial source 48 4m,sm+44st,a 52 Thompson, 1979 Guianacara sp. R Trombetas, PA 48 4m,sm+44st.a 52 2 cr. Feldberg et al., 1990 Gymnogeophagus gymnogenys Jacui/Tramandaí, RS 48 4m,sm+44st,a 52 Peixoto and Erdtmann, 1988 Gymnogeophagus balzanii Miranda, MS 24- 48 2m,sm+46st,a 50 2 cr. Feldberg and Bertollo, 1984; 26 1985b Gymnogeophagus balzanii R. Paraná, Argentina 48 2m,sm+46st,a 50 2 cr. Roncati et al., 1996 Gymnogeophagus labiatus Jacui/Tramandaí, RS 48 4m,sm+44st,a 52 2 cr. Peixoto and Erdtmann, 1988 Gymnogeophagus lacustris Jacui/Tramandaí, RS 48 4m,sm+44st,a 52 Peixoto and Erdtmann, 1988 Gymnogeophagus rhabdotus Jacui/Tramandaí, RS 48 4m,sm+44st,a 52 Peixoto and Erdtmann, 1988 Gymnogeophagus sp. n. R. Paraná, Argentina 48 Roncati et al., 2000 Mikrogeophagus ramirezi 24 64 Scheel, 1973 Mikrogeophagus ramirezi* 24 Post, 1965 Satanoperca acuticeps Rio Peixe-boi, PA 48 4 cr. Farias et al., 2000b Satanoperca jurupari Marchantaria and 48 6m,sm+42st,a 54 4 cr. Salgado et al., 1994 Catalão, AM Satanoperca jurupari Catalão, AM 48 4m,sm+44st,a 52 4 cr. Mendonça et al., 1999 5m,sm+43st,a 53 6m,sm+42st,a 54

293 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Satanoperca jurupari* Commercial source 48 4m,sm+44st,a 52 Thompson, 1979 Satanoperca jurupari* Amazônia 48 Moreira Filho, et al., 1980 Satanoperca pappaterra Rio Paraná 48 6m,sm+42st,a 54 2 cr. Martins et al., 1995

Cichlasomatinae Acaronia nassa Marchantaria and 50 50st,a 50 2 cr. Salgado et al., 1994 Catalão, AM Aequidens metae 48 6m,sm+42st,a 54 Thompson, 1979 Aequidens plagiozonatus R Paraná, PR 48 2 cr. Martins-Santos et al., 1990 Aequidens pulcher 24 82 Scheel, 1973 Aequidens sp. Amazônia 48 48st,a 48 2 cr. Salgado et al., 1995 Aequidens tetramerus Rio Peixe-boi, PA 48 2 cr. Farias et al., 2000b Amphilophus citrinellus* 24 82 Scheel, 1973 Amphilophus citrinellus* 48 36m,sm+12st,a 84 Nishikawa et al., 1973 Amphilophus citrinellus* 48 96 Zahner, 1977 Amphilophus citrinellus* 48 8m,sm+40st,a 56 Thompson, 1979 Amphilophus macracanthus* 24 Hinegardner and Rosen, 1972 Amphilophus macracanthus* 24 Scheel, 1973 Amphilophus macracanthus* 48 96 Zahner, 1977 Amphilophus macracanthus* 48 6m,sm+42st,a 54 Thompson, 1979 Archocentrus centrarchus* 48 6m,sm+42st,a 54 Thompson, 1979 Archocentrus nigrofasciatus* 24 96 Scheel, 1973 Archocentrus nigrofasciatus* 48 96 Zahner, 1977 Archocentrus nigrofasciatus* R Cuarto, Costa Rica 48 4m,sm+44st,a 52 Thompson, 1979 Archocentrus septemfasciatus* R Cuarto, Costa Rica 48 6m,sm+42st,a 54 Thompson, 1979 Archocentrus spilurus* 24 Scheel, 1973 Bujurquina sp I. Mindú, AM 48 8m,sm+40st,a 56 Mendonça (Pers. Comml) Bujurquina vittata Misiones, Argentina 44 Roncati et al., 2000

294 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Bujurquina vittata* 44 26m,sm+18st,a 70 Thompson, 1979 Caquetaia kraussii* 50 6m,sm+44st,a 56 Thompson, 1979 Caquetaia spectabilis Amazonas, Brasil 50 50st,a 50 5cr. Salgado et al., 1995 Cichlasoma amazonarum I. Mindú, AM 48 2m,sm+46st,a 50 3 cr. Salgado et al., 1995 Cichlasoma beani Mexico 48 6m,sm+42st,a 54 Thompson, 1979 Cichlasoma bimaculatum 44 44st,a 44 Santos et al., 1998 Cichlasoma bimaculatum 48 6m,sm+42st,a 54 Thompson, 1979 Cichlasoma dimerus Misiones, Argentina 48 Roncati et al., 2000 Cichlasoma facetum Uruguai 24 48 8m,sm+40st,a 56 Oyhenart-Perera et al., 1975 Cichlasoma facetum Registro, SP 24 48 10m,sm+38st,a 58 2 cr. Feldberg and Bertollo, 1985a,b Cichlasoma facetum Rio Claro, SP 24 48 10m,sm+38st,a 58 2 cr. Feldberg and Bertollo, 1985a,b Cichlasoma facetum S Cachoeira, São Mateus 48 10m,sm+38st,a 58 2 cr. Quijada and Cestari, 1998 do Sul, PR Cichlasoma octofasciatus 48 96 Zahner, 1977 Cichlasoma octofasciatus 48 6m,sm+42st,a 54 Thompson, 1979 Cichlasoma paranaense Guaravera, Londrina, PR 48 14m,sm+34st,a 62 6cr. Loureiro and Dias, 1998

Cichlasoma paranaense Rio Paraná, PR 48 20m,sm+28st,a 68 2 cr. Martins et al., 1995 Cichlasoma portalegrense* 24 82 Scheel, 1973 Cichlasoma salvini 52 104 Zahner, 1977

Cichlasoma salvini Belize 52 28m,sm+24st,a 80 Thompson, 1979 Cichlasoma sp. A 24 Scheel, 1973 Cichlasoma sp. C R Paraguai, MT 46 Rezende et al., 1996 Cichlasoma trimaculatus 48 6m,sm+42st,a 54 Thompson, 1979 Cleithracara maronii* 24 82 Scheel, 1973 Cleithracara maronii* 50 100 Zahner, 1977 Herichthys cyanoguttatus* 48 94 Zahner, 1977 Herichthys cyanoguttatus* Mexico 48 6m,sm+42st,a 54 Thompson, 1979

295 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Herichthys labridens S. Rioverde, Mexico 48 6m,sm+42st,a 54 Thompson, 1979 Herichthys minckleyi* Mexico 48 6m,sm+42st,a 54 Thompson, 1979 Heros severus* 24 Post, 1965: Scheel, 1973 Heros sp 24 Post, 1965 Heros sp 24 Scheel, 1973 Heros sp Marchantaria and 48 6m,sm+42st,a 54 2 cr. Salgado et al., 1994 Catalão, AM Herotilapia multispinosa 48 96 Zahner, 1977 Herotilapia multispinosa Commercial source 48 6m,sm+42st,a 54 Thompson, 1979 Hypselecara coryphaenoides* 48 6m,sm+42st,a 54 Thompson, 1979 Laetacara curviceps 19 Scheel, 1973 Laetacara curviceps* 19 Scheel, 1973 Mesonauta festivus Médio R. Negro 48 12m,sm+36st,a 60 4 cr. Santos et al., 2001 Mesonauta festivus* 24 Scheel, 1973

Mesonauta festivus* 48 96 Zahner, 1977 Mesonauta festivus* 48 8m,sm+40st,a 56 Thompson, 1979 Mesonauta insignis Baixo e Médio R. Negro 48 12m,sm+36st,a 60 4 cr. Santos et al., 2001 Nandopsis tetracanthus* Re San Juan, Cuba 48 6m,sm+42st,a 54 Ráb et al., 1983 Nannacara anomala 24 Post, 1965 Nannacara anomala 22 Scheel, 1973 Nannacara anomala 44 18m,sm+26st,a 62 Thompson, 1979 Neetroplus nematopus 48 8m,sm+40st,a 56 Thompson, 1979 Parachromis dovii R Cuarto, Costa Rica 48 8m,sm+40st,a 56 Thompson, 1979 Parachromis managuensis* 48 96 Zahner, 1977 Parachromis managuensis* 48 6m,sm+42st,a 54 Thompson, 1979

296 Table 13.1 (Contd.) Subfamily Species Locality n 2n KF FN NOR Reference Pterophyllum scalare* 24 Post, 1965 Pterophyllum scalare 24 Scheel, 1973 Pterophyllum scalare Commercial source 48 4m,sm+44st,a 52 Thompson, 1979 Pterophyllum scalare Amazônia, Brasil 48 4m,sm+44st,a 52 2 cr. Krychanã et al., 1996 Symphysodon aequifasciatus 60 44m,sm+16st, a 104 Ohno and Atkin, 1966 Symphysodon aequifasciatus 30 116 Scheel, 1973 Symphysodon aequifasciatus 60 58m,sm+2st,a 118 Thompson, 1979 Symphysodon aequifasciatus R.Amazonas, Tefé 60 44m,sm+16micr. 104 5cr. Salgado et al., 1995 Symphysodon aequifasciatus Amazônia, Brasil 60 42m,sm+18 micr 102 Salgado et al., 1996b citótipos: A e B Symphysodon aequifasciatus Manacapuru, AM 60 42m,sm+18micr 102 5 cr. Mesquita et al., 2000 Symphysodon discus Amazônia, Brasil 60 42m,sm+18micr 102 2 cr. Salgado et al., 1994 Symphysodon discus Amazônia, Brasil 60 48m,sm+12micr 108 2 cr. Salgado et al., 1996a 46m,sm+14micr 106 Uaru amphiacanthoides 46 8m,sm+38st,a 54 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, TMO- 4C4) 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 two- thirds 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 Af- rican 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 be- fore 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; Martins- Santos 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).

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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 inter- and 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 dis- tinct 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 interme- diate 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 Afri- can 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.

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