Evolutionary dynamics of repetitive DNA in semaprochilodus (characiformes, prochilodontidae): a fish model for sex chromosome differentiation.

Original Article Sex Dev 2013;7:325–333 DOI: 10.1159/000356691

Accepted: October 16, 2013 by M. Schmid Published online: November 28, 2013

Evolutionary Dynamics of Repetitive DNA in Semaprochilodus (Characiformes, Prochilodontidae): A Fish Model for Sex Chromosome Differentiation M.L. Terencio c C.H. Schneider a M.C. Gross a M.R. Vicari d I.P. Farias b K.B. Passos b E. Feldberg c

Key Words Chromosomal painting · FISH · Microsatellites · Repetitive sequences · Transposable elements · ZZ/ZW

radation of genetic activities and the differentiation of protosex chromosomes, evolving into the heteromorphic ZW pair observed in S. taeniurus. © 2013 S. Karger AG, Basel

Abstract Distribution of 6 microsatellites and 5 transposable elements on the chromosomes of Semaprochilodus taeniurus and S. insignis, commonly referred to as Jaraqui, was performed using their physical mapping with fluorescence in situ hybridization. In this study, we aim to understand the evolutionary dynamics in genomes of S. taeniurus and S. insignis by comparing the position, abundance and contribution of the repetitive sequences in the origins and differentiation of a ZZ/ZW sex chromosome system in S. taeniurus. Results revealed that distribution patterns of repetitive DNAs along the chromosomes varied considerably. Hybridization signals were observed on several autosomes in both species; however, in S. taeniurus genome, the repetitive sequences were more abundant. In addition, large clusters of known repetitive sequences were detected in sex chromosomes of S. taeniurus. This observation is notable because the accumulation of repetitive DNAs could reflect the deg-

Several studies on vertebrates revealed peculiarities about evolution and speciation [Pokorná et al., 2011; Schemberger et al., 2011; Gontan et al., 2012; Takehana et al., 2012; Schneider et al., 2013a, b]. In general, eukaryotic genomes, including those of fishes, are composed mostly of multiple families of tandem repetitive sequences (microsatellites, minisatellites and rDNA) and scattered sequences (transposable elements) that are considered determinant factors during speciation due to their high abundance and rapid evolutionary change [Fischer et al., 2004; Volff, 2005]. Satellite DNAs, for example, organized in blocks of thousands of copies in the genome mainly occur in the centromeric and telomeric regions of the chromosomes, indicating that they play an important role in the structure, stability and segregation of chromosomes [Ferree and Prasad, 2012]. Mobile or transposable elements are considered the drivers of genome evolution

© 2013 S. Karger AG, Basel 1661–5425/13/0076–0325$38.00/0 E-Mail [email protected] www.karger.com/sxd

Maria Leandra Terencio Laboratório de Genética Animal, Instituto Nacional de Pesquisas da Amazônia Av. André Araújo, 2936 Manaus, AM 69011-970 (Brazil) E-Mail leandrabio2 @ gmail.com

Downloaded by: Univ. of California Santa Barbara 198.143.33.33 - 2/26/2016 12:48:37 AM

a Laboratório de Citogenômica Animal and b Laboratório de Evolução e Genética Animal, Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, and c Laboratório de Genética Animal, Instituto Nacional de Pesquisas da Amazônia, Manaus, and d Laboratório de Citogenética e Evolução, Departamento de Biologia Estrutural, Molecular e Genética, Universidade Estadual de Ponta Grossa, Ponta Grossa, Brazil

Isolated Repetitive sequences clone

Similarity or repeat motif GenBank accession

SinH05 SinC01 SinG08 SinC08 SinG09 SinG02 Sin07 Ste4 Ste21 Ste20 –

(CA)22 (GA)20 (GT)17 (CT)26 (CT)14GT(CT)5(CG)2(CT)9 (GT)9CA(GT)7CG(GT)19 ERV2 Tc1_FR2 L2_2 Rex1–9_XT Rex3

microsatellite microsatellite microsatellite microsatellite microsatellite microsatellite DNA transposon DNA transposon non-LTR retrotransposon non-LTR retrotransposon non-LTR retrotransposon

HM147858 HM147844 HM147856 HM147847 HM147857 HM147855 JX848381 unpublished unpublished unpublished –

in several groups because, unlike satellite sequences that are usually more abundant in heterochromatic regions, they have a more uniform distribution pattern and often occur in euchromatic regions [Eickbush and Furano, 2002]. In Neotropical fishes, all known classes of these elements have been identified, and it is believed that the elements are responsible for numerous chromosomal rearrangements, as observed in the genera Gymnotus [da Silva et al., 2011], Cichla [Valente et al., 2011] and Symphysodon [Gross et al., 2009]. Thus, repetitive DNAs have been widely applied as physical chromosomal markers in comparative studies for locating chromosomal rearrangements, identifying and characterizing sex chromosomes and analyzing chromosomal evolution in Neotropical fishes [Gross et al., 2009; Machado et al., 2011; Schemberger et al., 2011; Terencio et al., 2012a, b; Schneider et al., 2013a, b]. The genus Semaprochilodus (popularly known as Jaraqui) consists of 6 species of fishes (S. brama, S. insignis, S. kneri, S. laticeps, S. taeniurus, and S. varii) that are endemic to the Amazon region and are important to Amazonian fish trade [Castro and Vari, 2003]. In relation to cytogenetics, species of the genus Semaprochilodus demonstrate conserved chromosome numbers (2n = 54) and chromosome morphologies of the meta- and submetacentric type. The character encountered with the greatest divergence until now in terms of the karyotypic macrostructure of the species of this genus is the presence of a ZZ/ZW sex chromosome system in S. taeniurus. Molecular and cytogenomic analyses [Passos et al., 2010; Terencio et al., 2012a, b] have revealed that a fraction of the S. taeniurus and S. insignis genomes contains a wide variety of repetitive sequence types, such as 326

Sex Dev 2013;7:325–333 DOI: 10.1159/000356691

transposons and retrotransposons. The presence of repetitive sequences is important because these sequences could have influenced the differentiation of the ZW heteromorphic pair in S. taeniurus and be active in the genome of other fish species [Terencio et al., 2012b]. Thus, in the present study, we present an extensive physical chromosomal map of repetitive sequences, such as previously identified microsatellites and transposable elements [Passos et al., 2010; Terencio et al., 2012b], to compare the position and abundance of the different classes of these sequences in the genomes of S. taeniurus and S. insignis (which does not have heteromorphic sex chromosomes) and to understand the evolutionary dynamics of the genomes of these species. In addition, we discuss the influence of these sequences on the evolution of the sex determination system (ZW) in S. taeniurus because the sequences appear to be associated with the differentiation of a heteromorphic ZW pair observed in this species.

Material and Methods Ten specimens of S. insignis (6 females and 4 males) and 12 specimens of S. taeniurus (7 females and 5 males), collected with the authorization of ICMBio SISBIO (10609-1/2007) at the confluence of the Negro/Solimões Rivers (Amazonas Brazil) and the Amazonas/Tapajós Rivers (Pará Brazil), were cytogenetically examined. The fish were anesthetized in ice-cold water and sacrificed. Voucher specimens were deposited in the INPA Animal Genetics Laboratory fish collection (10034, 10037, 10047, and 10696). Chromosomal preparations were obtained from anterior kidney cells using an in vivo colchicine treatment [Bertollo et al., 1978]. The heterochromatin was analyzed by C-banding [Sumner, 1972]. Genome Sequences Six microsatellites, including 4 dinucleotide and 2 imperfect, isolated from the genome of S. insignis [Passos et al., 2010], and 5 mobile elements previously sequenced and identified in the genomes of S. taeniurus and S. insignis were mapped by fluorescence in situ hybridization (FISH) on S. insignis and S. taeniurus chromosomes in metaphase (table 1). The accession numbers of Tc1_ FR2, L2_2 and Rex1–9_XT transposons were not included in this paper because the GenBank does not accept sequences less than 200 bp in length. The retroelement Rex3 was recovered via PCR using the primers RTX3-F3 5′-CGG TGA YAA AGG GCA GCC CTG-3′ and RTX3-R3 5′-TGG CAG ACN GGG GTG GTG GT-3′ [Volff et al., 1999]. Fluorescence in situ Hybridization The repetitive sequence probes for S. taeniurus and S. insignis were labeled with digoxigenin-11-dUTP (Dig-Nick Translation mix; Roche) and/or Biotin-16-dUTP (Biotin Nick Translation mix; Roche) by nick translation reactions following the manu-

Terencio /Schneider /Gross /Vicari /Farias / Passos /Feldberg


Table 1. Repetitive sequences hybridized on S. insignis and S. taeniurus chromosomes

Microscopy/Image Processing Hybridized chromosomes were analyzed using an Olympus BX51 epifluorescence microscope, and the images were captured with a digital camera (Olympus DP71), using the Image-Pro MC 6.3 software.

Results

Hybridization of Repetitive DNA Sequences in S. taeniurus FISH on S. taeniurus cells in metaphase indicated positive hybridization signals for all repetitive sequences tested; however, these sites exhibited differences in chromosomal locations (fig. 1). The microsatellite (CA)22 was mainly found in the terminal regions of several chromosomes, in the centromeric and telomeric region of the Z chromosome and interstitially on the long arm of the W chromosome (fig. 1a). The microsatellite (GA)20 is present in the centromeric and/or interstitial regions of most autosomes, and one homologous pair showed hybridization signals at both telomeres (arrows). On the W chromosome, hybridization signals were found in the pericentromeric region of both arms (fig. 1b). The microsatellite marker (CT)26 hybridized to centromeric, interstitial and/or telomeric regions on most chromosomes, including the sex chromosomes (arrows) (fig. 1c). Conspicuous hybridization signals of the microsatellite (CT)14GT(CT)5(CG)2(CT)9 probe were observed on the long arm of the W chromosome and the telomeric region of the Z chromosome (arrows). Additionally, weaker signals for these microsatellites were found in terminal and centromeric regions of several chromosomes (arrows) (fig. 1d). The microsatellite (GT)17 was identified in the centromeric and interstitial regions of the long arm of the W chromosome, beyond the terminal region of the Z chromosome and one autosome Evolutionary Dynamics of Repetitive DNA in Semaprochilodus

Table 2. Comparison of FISH results with probes prepared from

repetitive sequences on the S. insignis and S. taeniurus chromosomes Similarity or repeat motif

S. taeniurus

S. insignis

(CA)22 (GA)20 (GT)17 (CT)26 (CT)14GT(CT)5(CG)2(CT)9 (GT)9CA(GT)7CG(GT)19 ERV2 Tc1_FR2 L2 Rex1 – 9_XT Rex3

+ + + + + + + + + + +

+ + + + – – – – – + +

+ = Hybridization signals; – = absence of hybridization.

(fig. 1e). The microsatellite (GT)9CA(GT)7CG(GT)19 was located only in the interstitial region on the long arm of the W chromosome (fig. 1f). The repetitive sequence ERV2 classified as endogenous retrovirus was identified only in the terminal region of the long arm of the W chromosome (fig. 1g). The retrotransposon L2 showed positive hybridization signals in the centromeric region of some chromosomes, including the sex chromosomes Z and W (fig. 1h). The retroelement Rex1 was compartmentalized to the centromeric or interstitial regions of some chromosome pairs, but its location was scattered on the sex chromosomes (fig. 1i). The retroelement Rex3 showed scattered localization on all autosomes, and certain signs were more conspicuous in the terminal and interstitial regions; this pattern was also evident on the Z and W sex chromosomes (fig. 1j). The transposable element Tc1 was found in the centromeric and terminal regions of certain chromosomes and in the interstitial region of the long arm of the Z chromosome. No hybridization signal was evident on the W chromosome (fig. 1k). The C-banding technique revealed that heterochromatin is located in the centromeric regions of most chromosomes and in terminal regions of certain chromosomes. On the Z chromosome, the heterochromatin was found in the centromeric and terminal regions of the long arm. The W chromosome showed large amounts of heterochromatin along its chromosomal length (fig. 1l).

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facturer’s instructions. FISH was performed on mitotic chromosome spreads [Pinkel et al., 1986]. The metaphase chromosome slides were incubated with RNase (10 μg/ml) for 1 h at 37 ° C. After denaturation of chromosomal DNA in 70% formamide, spreads were dehydrated in cold alcohol solutions (70, 85 and 100%) for 5 min. The FISH procedure was performed under high stringency conditions (2.5 ng/μl of each probe, 50% formamide, 10% dextran sulfate, and 2× SSC at 37 ° C for 18 h). Posthybridization washes were carried out at 42 ° C in 0.2× SSC/15% formamide for 20 min, followed by a second wash in 0.5% Tween solution for 5 min. The antibodies antidigoxigenin-rhodamine (Roche) and Alexa-Fluor-streptavidin 488 (Life Technologies) were used to detect the signals. The chromosomes were counterstained with DAPI (2 μg/ml), in Vectashield mounting medium (Vector).

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Fig. 1. S. taeniurus chromosomes in metaphase, hybridized with microsatellite sequences (a–f) and transposable elements (g–k) (for probes, see table 1). The chromosomes were counterstained with DAPI, and the probes were labeled with biotin (green) and digoxigenin (red). Furthermore, location of the constitutive heterochromatin in this species is shown (l). Letters mark the sex chromosomes Z and W. For closer details, see Results section.

Hybridization of Repetitive DNA Sequences in S. insignis In S. insignis, not all repetitive sequences showed positive hybridization signals (table 2). The microsatellite (CA)22 was predominantly observed in the centromeric region of several chromosomes including one large metacentric homolog (arrow) and in the terminal region of a single chromosomal pair (fig. 2a). The microsatellite (GA)20 was found in the centromeric and/or interstitial regions of several chromosomes, and one homologous pair (arrows) showed bitelomeric and centromeric labeling (fig. 2b). The microsatellite marker (CT)26 hybridized in centromeric and/or telomeric regions in 10 chromosome pairs, as well as in one of the large metacentric ho-

mologs in the centromeric region (fig. 2c, arrow). The (GT)17 marker labeled the terminal regions of 9 chromosomes and the centromeric region of only one chromosome (fig. 2d, arrow). In this species, only the retrotransposons Rex1 and Rex3 could be found by the FISH technique. The transposable element Rex1 (fig. 2e) showed a compartmentalized distribution in the centromeric regions of most chromosomes and in the terminal regions of 2 larger chromosomes corresponding to the first metacentric pair. Moreover, the retroelement Rex3 (fig. 2f) showed a scattered distribution pattern and was found in all chromosomal regions of most of the chromosome complement. The C-banding technique showed that heterochromatin

Evolutionary Dynamics of Repetitive DNA in Semaprochilodus

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Fig. 2. S. insignis chromosomes in metaphase, hybridized with microsatellite sequences (a–d) and transposable elements (e, f) (for probes, see table 1). The chromosomes were counterstained with DAPI, and the probes were labeled with biotin (green) and digoxigenin (red). Moreover, location of the constitutive heterochromatin in this species is demonstrated (g). For closer details, see Results section.

Discussion

Chromosomal Distribution of Repetitive Sequences on Autosomes Comparison of the heterochromatic patterns and physical chromosomal maps of the repetitive sequences from S. taeniurus and S. insignis showed that they occur more frequently in heterochromatic regions, but hybridization sites were also found in euchromatic regions, suggesting that a portion of these sequences play a functional role in the genome. The Encyclopedia of DNA Elements has shown that the genome – the noncoding majority of it – is rich with functional elements. The noncoding regions contain docking sites where proteins can stick and switch genes on or off, regions that encode RNA molecules, more than 70,000 promoters that control the transcription of nearby genes, more than 400,000 enhancers that influence the activity of other genes, sometimes across great distances, and regions that affect how DNA is folded and packaged [ENCODE Project Consortium et al., 2012]. In general, the chromosomal hybridization of microsatellites indicated that they accumulate more intensely in the centromeric and terminal regions of the autosomes in both S. insignis and S. taeniurus. However, comparative analysis revealed that certain of these sequences occur in different chromosomal regions of these species. In S. taeniurus, the microsatellite (CA)22 was mainly found in the terminal regions of the chromosomes, whereas it was mainly found in the centromeric regions of the same chromosomes in S. insignis. This information is interesting since S. taeniurus showed large terminal label, not observed in S. insignis in FISH using a Cot1 DNA probe (renaturation kinetics). These results suggest that these sequences are involved in the structural formation of the centromere and telomere, which characteristically exhibit a large number of tandem repetitive sequences. The repetitive nature of these regions extends beyond the classically defined boundaries of centromeric and telomeric sequences to influence the frequency of structural rearrangements in surrounding regions. These regions are hotspots for the insertion or retention of repeat sequences and have been identified in the centromeric satellite DNA of various fish species [Canapa et al., 2002; Eichler and Sankoff, 2003]. 330

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In S. insignis, the microsatellites (CA)22 and (CT)26 were found in the centromeric region of only one of the homologs of the first metacentric pair. This type of discordant labeling in homologs could be due to sequence duplication events in only one of these homologs, which would allow the identification of these clusters by FISH. The distribution of transposable elements in the genome of most organisms is uniform, occurring in both euchromatic and heterochromatic regions [Volff et al., 2003; Fischer et al., 2004]. The physical chromosomal mapping of this class of repetitive sequences corroborated this finding and revealed distinct patterns of abundance and location in different species. The transposable elements L2 and Tc1 only showed hybridization signals on the autosomes of S. taeniurus, indicating that there were a greater number of copies of these elements in the genome of this species. Moreover, the retrotransposons Rex1 and Rex3 were found in the genome of both species and exhibited the same distribution pattern, with Rex1 located in compartmentalized blocks in the centromeric regions of a few chromosomes and Rex3 in the subterminal and terminal regions of most chromosomes. These results are interesting because they reflect evolutionary conservation of these elements in the genomes of both species. The compartmentalization observed in centromeric and terminal regions suggests 2 possibilities: (1) transposition events are more common in the heterochromatic regions, and (2) repetitive sequences are massively eliminated in gene-rich regions [Fischer et al., 2004]. Recently, the hybridization of the retroelements Rex1, Rex3 and Rex6 in Neotropical cichlids also revealed a conserved pattern in this group of fish [Schneider et al., 2013b]. The genome of fishes contains innumerable retrotransposon families that are widely studied because of their impact on genomes: chromosomal rearrangements, differentiation of sex chromosomes and, consequently, speciation [Ozouf-Costaz et al., 2004]. However, certain transposable elements, such as the telomeric retrotransposons of Drosophila, are apparently beneficial to the host, and it is hypothesized that during evolution, many of these elements may have performed new cell functions in the genome [Fischer et al., 2004; Biémont and Vieira, 2006]. Studies examining scattered repetitive elements in insect genomes have also shown that after the invasion phase, they tend to be silenced and subsequently undergo molecular deterioration until incorporation into the host genome [Fernández-Medina et al., 2012]. In the molecular deterioration phase, the element becomes inactive and progressively accumulates mutations, insertions and deletions at neutral Terencio /Schneider /Gross /Vicari /Farias / Passos /Feldberg


is located in the centromeric regions of most of the chromosomes and in the pericentromeric and terminal regions of several chromosomes (fig. 2g).

rates until it completely loses its identity or is lost in the host genome [Fernández-Medina et al., 2012]. In general, the comparative analysis performed in this study revealed that the genome of S. taeniurus is richer in heterochromatin and repetitive sequences, which may have significantly contributed to a genomic differentiation between these species.


Fig. 3. Schematic ideogram of the S. taeniurus sex chromosomes,

highlighting the distribution pattern of the repetitive sequences identified by FISH. Regions in gray represent the location of the constitutive heterochromatin.

Fig. 4. The localized pattern of the repetitive sequences identified

by FISH and the location of the constitutive heterochromatin (Cband) in the S. taeniurus sex chromosomes (Z and W).

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Chromosomal Distribution of Repetitive Sequences in the Sex Chromosomes of S. taeniurus S. taeniurus is the only species of the Prochilodontidae family that has a ZW sex determination system. Morphologically, the W chromosome is much larger than its Z homolog and contains a large amount of heterochromatin [Feldberg et al., 1987; Terencio et al., 2012a]. The W chromosome of S. taeniurus features a large number of tandem and scattered repetitive sequences, and it has been suggested that these sequences may have contributed to the evolution of the sexual system in this species [Terencio et al., 2012b]. Several hypotheses have been proposed to explain the origin of the sex chromosomes. Their differentiation from an autosomal pair and/or the partial or total degradation of sex-specific chromosomes [Muller, 1964; Ohno, 1967] are the most accepted hypotheses for many groups of organisms. One of these mechanisms proposed for the differentiation of autosome pairs into sex chromosomes involves a gradual reduction in their recombination [Brooks, 1988]. This process can be strongly influenced by the distribution of retrotransposons in the genome, indicating that the major force driving the evolution of sex chromosomes are repetitive sequences, remodeling euchromatic chromosome structures into heterochromatic [Steinemann and Steinemann, 2005; Böhne et al., 2012]. It is possible that the suppression of recombination and the degradation of genetic activities of the protosex chromosomes of S. taeniurus promoted the accumulation of heterochromatin in the W chromosome that has significantly increased in size due to the accumulation of repetitive DNAs, with the consequent differentiation of the ZZ/ZW system of sex chromosomes. Data accumulated from recent studies indicated that repetitive sequences have had significant influence on the evolution of genomes, particularly by controlling gene activity, and have been promoters of sex chromosome differentiation in a number of organisms, including fish such as Hoplias malabaricus [Cioffi and Bertollo, 2010], Characidium spp. [Machado et al., 2011], Oryzias javanicus [Takehana et al., 2012], and members of the Parodontidae [Schemberger et al., 2011].

The results obtained in the present study support this hypothesis because large clusters of known repetitive sequences were detected in the sex pair, especially in the W chromosome. Furthermore, a comparative analysis indicated that some of the repetitive sequences invaded euchromatic regions, although the majority of these sequences occur in heterochromatic regions (fig. 3). The accumulation of these repetitive sequences in gene-rich regions could reflect gradually reduced crossing-over between protosex chromosomes, evolving in the heteromorphic ZW pair. Physical chromosomal mapping of the microsatellites in the sex chromosomes revealed that these sequences occurred in the centromeric and telomeric regions of the Z chromosome and, more intensely, in the pericentromeric and interstitial regions of the W chromosome (fig. 4). Generally, the accumulation of microsatellites precedes the evolution of heteromorphic sex chromosomes. It is possible that the accumulation of microsatellites plays an important role in the evolution of sex chromosomes because of their ability to adopt unusual DNA conformations, including hairpins, triplex and tetraplex structures [Wells et al., 2005]. Transposable elements have been identified on the sex chromosomes of many organisms, and the results suggest that massive mobilization of these elements may be associated with genetic instabilities that evolved on the heteromorphic chromosome pair. The accumulation of

transposable elements is most likely an early effect of restricted recombination; therefore, increased DNA content may be one of the first changes affecting sex chromosomes [Larin et al., 1994; Desset et al., 2003; Bartolomé and Maside, 2004; Feschotte and Pritham, 2007; Gontan et al., 2012; Terencio et al., 2012b]. Thus, the results found in the present study suggest a significant role of repetitive DNA in the evolution of sex chromosomes in S. taeniurus. Additional studies will be necessary to provide further insights into the possible structural and functional roles that repetitive DNA sequences play in Semaprochilodus spp. genomes, with particular reference to evolutionary mechanisms that remodeled the W chromosome of the S. taeniurus during evolution. Genomic research of other fish species from the Prochilodontidae family can provide important information regarding karyotype evolution in this group of fish.

Acknowledgements This study was supported by the National Council for Scientific and Technological Development (CNPq – 141660/2009-0 and 554057/2006-9 to I.P.F.), the National Amazon Research Institute/ Genetic, Conservations and Evolutionary Biology (INPA/GCBEV), the State of Amazonas Research Foundation (FAPEAM), and the Centre for Studies of Adaptation to Environmental Changes in the Amazon (INCT ADAPTA,FAPEAM/CNPq 573976/2008-2 and PRONEX/FAPEAM/CNPQ 003/2009).

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Transmission rate variation among three B chromosome variants in the fish Prochilodus lineatus (Characiformes, Prochilodontidae).

New approach data in electric fish (Teleostei: Gymnotus): sex chromosome evolution and repetitive DNA.

Development and characterization of 24 polymorphic microsatellite loci for the freshwater fish Ichthyoelephas longirostris (Characiformes: Prochilodontidae).

Chromosome mapping of repetitive sequences in four Serrasalmidae species (Characiformes).

W Chromosome Dynamics in Triportheus Species (Characiformes, Triportheidae): An Ongoing Process Narrated by Repetitive Sequences.

Data on the multilocus molecular phylogenies of the Neotropical fish family Prochilodontidae (Teleostei: Characiformes).

Sex chromosome evolution: life, death and repetitive DNA.

Transmission Behavior of B Chromosomes in Prochilodus lineatus (Characiformes, Prochilodontidae).

Complete mitochondrial genome sequence of Prochilodus lineatus (Characiformes, Prochilodontidae).

ZW sex chromosome system in the endangered fish Lignobrycon myersi Miranda-Ribeiro, 1956 (Teleostei, Characiformes, Triportheidae).

In situ localization of (GATA)n and (TTAGGG)n repeated DNAs and W sex chromosome differentiation in Parodontidae (Actinopterygii: Characiformes).

Delimiting the origin of a B chromosome by FISH mapping, chromosome painting and DNA sequence analysis in Astyanax paranae (Teleostei, Characiformes).

Genomic organization of repetitive DNAs and its implications for male karyotype and the neo-Y chromosome differentiation in Erythrinus erythrinus (Characiformes, Erythrinidae).

Four new records of fish species (Cypriniformes: Nemacheilidae, Balitoridae; Characiformes: Prochilodontidae) and corrections of two misidentified fish species (Tetraodontiformes: Tetraodontidae; Beloniformes: Belonidae) in Yunnan, China.

Chromosome differentiation patterns during cichlid fish evolution.

Molecular characterization of repetitive DNA sequences from a B chromosome.

Evolutionary trends in the family Curimatidae (Characiformes): inferences from chromosome banding.

The Evolutionary Tempo of Sex Chromosome Degradation in Carica papaya.

A Glimpse into the Satellite DNA Library in Characidae Fish (Teleostei, Characiformes).

Dynamic DNA underpins chromosome dynamics.

Organization of DYZ2 repetitive DNA on the human Y chromosome.

Neotropical fish-fruit interactions: eco-evolutionary dynamics and conservation.

On the potential of simple repetitive DNA for fingerprinting in clinical, forensic, and evolutionary dynamic studies.

Chromosomal mapping of repetitive DNAs in Triportheus trifurcatus (Characidae, Characiformes): insights into the differentiation of the Z and W chromosomes.