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Chromosome Differentiation Patterns During Cichlid Fish Evolution

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Chromosome Differentiation Patterns During Cichlid Fish Evolution Poletto et al. BMC Genetics 2010, 11:50 http://www.biomedcentral.com/1471-2156/11/50 RESEARCH ARTICLE Open Access ChromosomeResearch article differentiation patterns during cichlid fish evolution Andréia B Poletto1, Irani A Ferreira1, Diogo C Cabral-de-Mello1, Rafael T Nakajima1, Juliana Mazzuchelli1, Heraldo B Ribeiro1, Paulo C Venere2, Mauro Nirchio3, Thomas D Kocher4 and Cesar Martins*1 Abstract Background: Cichlid fishes have been the subject of increasing scientific interest because of their rapid adaptive radiation which has led to an extensive ecological diversity and their enormous importance to tropical and subtropical aquaculture. To increase our understanding of chromosome evolution among cichlid species, karyotypes of one Asian, 22 African, and 30 South American cichlid species were investigated, and chromosomal data of the family was reviewed. Results: Although there is extensive variation in the karyotypes of cichlid fishes (from 2n = 32 to 2n = 60 chromosomes), the modal chromosome number for South American species was 2n = 48 and the modal number for the African ones was 2n = 44. The only Asian species analyzed, Etroplus maculatus, was observed to have 46 chromosomes. The presence of one or two macro B chromosomes was detected in two African species. The cytogenetic mapping of 18S ribosomal RNA (18S rRNA) gene revealed a variable number of clusters among species varying from two to six. Conclusions: The karyotype diversification of cichlids seems to have occurred through several chromosomal rearrangements involving fissions, fusions and inversions. It was possible to identify karyotype markers for the subfamilies Pseudocrenilabrinae (African) and Cichlinae (American). The karyotype analyses did not clarify the phylogenetic relationship among the Cichlinae tribes. On the other hand, the two major groups of Pseudocrenilabrinae (tilapiine and haplochromine) were clearly discriminated based on the characteristics of their karyotypes. The cytogenetic mapping of 18S ribosomal RNA (18S rRNA) gene did not follow the chromosome diversification in the family. The dynamic evolution of the repeated units of rRNA genes generates patterns of chromosomal distribution that do not help follows the phylogenetic relationships among taxa. The presence of B chromosomes in cichlids is of particular interest because they may not be represented in the reference genome sequences currently being obtained. Background native to South India and the Middle East [4]. Mitochon- Teleost fishes have a successful history of diversification drial genome sequences indicate that cichlids are closely over the past 200 million years. The 23.000 species of related to the marine surfperches (Embiotocidae) and teleosts make up almost half of all living vertebrates [1]. damselfishes (Pomacentridae), but not as previously Perciformes represents the largest order of vertebrates thought, to wrasse and parrotfishes (Labridae and related with approximately 9.300 species. It includes more than families) [5]. Phylogenetic reconstructions are consistent 3.000 species of the family Cichlidae [1,2] that is one of with cichlid origins prior to Gondwanan landmass frag- the most species-rich families of vertebrates [3]. The nat- mentation 121-165 MYA, considerably earlier than the ural distribution of cichlid fishes is centered on Africa, first known cichlid fossils from Eocene [5]. Cichlid fishes Latin America and Madagascar, with only a few species found in the lakes of Africa have served as model systems for the study of evolution [4,6,7]. Several species have * Correspondence: [email protected] received increasing scientific attention because of their 1 UNESP - Universidade Estadual Paulista, Instituto de Biociências, Departamento de Morfologia, Botucatu, SP, Brazil great importance to tropical and subtropical aquaculture Full list of author information is available at the end of the article [8]. © 2010 Poletto et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Poletto et al. BMC Genetics 2010, 11:50 Page 2 of 12 http://www.biomedcentral.com/1471-2156/11/50 The family Cichlidae is a monophyletic group and the conserved with 2n = 44 chromosomes for most species limits and interrelationships of all four subfamilies and the presence of a large st/a typical chromosome (pair [Etroplinae (Indian and Madagascar), Ptychochrominae 2 in O. niloticus, pair 5 in T. mariae, pair 6 in T. mamfe) (Malagasy), Cichlinae (Neotropical region) and Pseudo- (Figure 1). Reduction in the number of chromosomes was crenilabrinae (African)] are well supported by molecular observed in T. mariae that shows 40 chromosomes with and morphological data [9]. The African (Pseudocre- the presence of two atypical metacentric chromosome nilabrinae) and Neotropical (Cichlinae) cichlids are both pairs (pairs 1 and 2) (Figure 1). monophyletic and represent sister groups [9]. The Afri- Most of the haplochromine species we analyzed had a can Pseudocrenilabrinae cichlids are often assigned into karyotype composed of 2n = 44 (Figure 1, Table 1). Asta- pelmatochromine, haplochromine and tilapiine groups totilapia burtoni had a karyotype composed of 40 chro- [10], but these groups are not recognized as valid taxo- mosomes, with 14 m/sm and 26 st/a chromosomes, and nomic units. The Neotropical cichlids (Cichlinae) are two large m/sm chromosome pairs (pairs 2 and 3) not monophyletic and are composed of 51 genera and 406 observed in other haplochromines (Figure 1, Table 1). All described species [11,12]. The most recently proposed the haplochromines have two typical large chromosome phylogeny of the Cichlinae denotes the tribes Cichlini, pairs, the first m/sm and the first st/a pairs. Retroculini, Astronotini, Chaetobranchini, Geophagini, When compared to the haplochromines and tilapiines, Cichlasomatini and Heroini [13]. the karyotype of Hemichromis bimaculatus (Hemichrom- The karyotypes of more than 135 species of cichlids ine) shows the same diploid number (2n = 44), but with have been determined. Although most species present a only two m/sm chromosome pairs (Figure 1, Table 1). A karyotype with 2n = 48, the diploid number ranges from large st/a (pair 3) and a large m/sm (pair 1) chromosome 2n = 32 to 2n = 60 [14] (See Additional File 1: Available were also observed. chromosomal data for the Cichlidae). African cichlids B chromosomes were detected in Haplochromis obliq- have a modal diploid number of 44 chromosomes uidens and Metriaclima lombardoi. One or two large whereas the Neotropical cichlids 2n = 48 chromosomes. metacentric B chromosomes were present in 38 out of 96 Even though chromosomal data are known for several analyzed specimens of H. obliquidens whereas one large B cichlid species, these data are not representative of the chromosome was detected in nine out of 22 animals sam- diversity of species in the group. Molecular cytogenetics pled for M. lombardoi (Table 1). approach to characterizing genome evolution has been Subfamily Cichlinae applied to only a few species, principally Oreochromis The karyotypes of Cichla species (Cichlini) and Retrocu- niloticus. The aim of this work was to obtain chromo- lus lapidifer (Retroculini) presented 2n = 48 st/a chromo- somal data for additional species of cichlids, including the somes (Figure 2, Table 2). The karyotype of Astronotus mapping of 18S ribosomal RNA (rRNA) genes, and to ocellatus (Astronotinae) presents 12 m/sm chromosomes compare these results to previous published chromo- and Chaetobranchus flavescens (Chaetobranchini) shows somal data and phylogenies, in order to correlate chro- 6 m/sm chromosomes (Figure 2, Table 2), both with 2n = mosomal rearrangements with particular phylogenetic 48. transitions during the evolutionary history of the family The karyotypes of Geophagini species are similar to Cichlidae. Chaetobranchini (Figure 2, Table 2). On the other hand, the karyotype of Apistogramma borelli presented a Results reduced number of chromosomes (2n = 46) and the pres- Basic cytogenetic analysis ence of a higher number of m/sm chromosomes (eight Subfamily Etroplinae pairs) compared to the non-geophagines (Figure 2). The karyotype of Etroplus maculatus consists of 46 chro- Among the Cichlasomatini analyzed, Laetacara dorsig- mosomes including 18 m/sm (meta/submetacentric), 18 era showed a reduced chromosome number (2n = 44) st/a (subtelo/acrocentric) and 10 microchromosomes with the presence of two outstanding large metacentric (Table 1, Figure 1). The most remarkable characteristics pairs (pairs 1 and 2) (Figure 2). of the E. maculatus karyotype were the presence of two Heroini showed the broadest range of karyotype con- outstanding large metacentric pairs, several small chro- figurations. The cichlids Heros efasciatus, Mesonauta fes- mosomal pairs identified as m/sm or st/a, and five pairs tivus, Parachromis managuensis and Pterophyllum of microchromosomes. scalare have 2n = 48 chromosomes with variations in the Subfamily Pseudocrenilabrinae number of m/sm and st/a chromosomes (Figure 2, Table In this work we sampled the tilapiines Oreochromis 2). The Symphysodon aequifasciatus karyotype is by far aureus, O. mossambicus, O. niloticus, O. tanganicae, Tila- the most derived of all cichlids, with a highly increased pia mamfe and T. mariae (Figure 1, Table 1). The karyo- number
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