Multiple Sex Chromosomes and Evolutionary Relationships in Amazonian Catfishes: The Outstanding Model of the Genus Harttia (Siluriformes: Loricariidae)

Abstract

The armored Harttia catfishes present great species diversity and remarkable cytogenetic variation, including different sex chromosome systems. Here we analyzed three new species, H. duriventris, H. villasboas and H. rondoni, using both conventional and molecular cytogenetic techniques (Giemsa-staining and C-banding), including the mapping of repetitive DNAs using fluorescence in situ hybridization (FISH) and comparative genomic hybridization (CGH) experiments. Both H. duriventris and H. villasboas have 2n = ♀56/♂55 chromosomes, and an X1X1X2X2 /X1X2Y sex chromosome system, while a proto or neo-XY system is proposed for H. rondoni (2n = 54♀♂). Single motifs of 5S and 18S rDNA occur in all three species, with the latter being also mapped in the sex chromosomes. The results confirm the general evolutionary trend that has been noticed for the genus: an extensive variation on their chromosome number, single sites of rDNA sequences and the occurrence of multiple sex chromosomes. Comparative genomic analyses with another congeneric species, H. punctata, reveal that the X1X2Y sex chromosomes of these species share the genomic contents, indicating a probable common origin. The remarkable karyotypic variation, including sex chromosomes systems, makes Harttia a suitable model for evolutionary studies focusing on karyotype differentiation and sex chromosome evolution among lower vertebrates.

Highly Rearranged Karyotypes and Multiple Sex Chromosome Systems in Armored Catfishes from the Genus Harttia (Teleostei, Siluriformes)

“… Representative idiograms of Harttia species from distinct Brazilian regions based on the distribution of rDNA sequences in their karyotypes, according to the present study, Blanco et al [ 8 ], and Sassi et al [ 11 ] data. The location of the 18S and 5S rDNA sites on the chromosomes are indicated in green and red, respectively.…”

“…In the Harttia genus, two multiple sex chromosome systems were previously described, the X 1 X 1 X 2 X 2 /X 1 X 2 Y one in H. punctata , H. duriventris, and H. villasboas and the XX/XY 1 Y 2 system in H. carvalhoi [ 8 , 11 ]. While the first one is well-represented among a variety of fish families [ 18 ], the XX/XY 1 Y 2 system is found in only a few fish species ( Table 3 ).…”

“…Furthermore, the chromosomal rearrangements in Harttia species culminated in different kinds of sex chromosome systems: ( i ) an XX/XY 1 Y 2 system in H. carvalhoi [ 9 ]; ( ii ) an X 1 X 1 X 2 X 2 /X 1 X 2 Y system in Harttia punctata , Harttia duriventris , and Harttia villasboas [ 10 , 11 ]; and ( iii ) a neo XX/XY system in Harttia rondoni [ 11 ]. In accordance with the two branches of Harttia species [ 7 ], these sex chromosome systems followed independent evolutionary origins [ 8 , 11 ]. While H. carvalhoi is grouped with H. kronei , H. longipinna , H. loricariformis , and some other species distributed in southern and southeastern Brazil, H. punctata , H. rondoni , H. duriventris , and H. villasboas are grouped in a different branch with other species from the north and northeast Brazilian drainages [ 7 ].…”

Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: state of the art and future challenges

“…Simultaneous hybridization of male and female whole-genome probes to chromosome spreads may reveal differentially painted regions, which can correspond to non-recombining loci accumulating sex-limited or -enriched sequences. To date, this method has been used in diverse fishes with multiple sex chromosomes with varying success [51,52,[108][109][110]. One drawback, however, of CGH is its low resolution as it fails to provide detailed sequence composition of the sex-specific region.…”

Fish Cytogenetics: Present and Future

“…In details, the investigation of new species and the integration of data from literature showed an extensive variability of the chromosome number in species of the genus Harttia and the occurrence of different sex chromosome systems. These features make Harttia a suitable model to study sex chromosome evolution in fishes [ 23 ].…”