Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae)
Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper th...
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| Published in | Frontiers in genetics Vol. 10; p. 678 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Switzerland
Frontiers Media S.A
02.08.2019
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1664-8021 1664-8021 |
| DOI | 10.3389/fgene.2019.00678 |
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| Abstract | Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper the karyotype evolution of specific groups, especially the historically neglected small-sized ones. Representatives of the family Lebiasinidae (Characiformes) are a notable example, where only a few cytogenetic investigations have been conducted thus far. Here, we aim to elucidate the evolutionary processes behind the karyotype differentiation of
species on a finer-scale cytogenetic level. To achieve this, we applied C-banding, repetitive DNA mapping, CGH and WCP in
and
. Our results showed 2n = 42 in both sexes of
, while the difference in 2n between male and female in
(♂41/♀42) stands out due to the presence of a multiple X
X
Y sex chromosome system, until now undetected in this family. As a remarkable common feature, multiple 18S and 5S rDNA sites are present, with an occasional synteny or tandem-repeat amplification. Male-
.-female CGH experiments in
highlighted the accumulation of male-enriched repetitive sequences in the pericentromeric region of the Y chromosome. Inter-specific CGH experiments evidenced a divergence between both species' genomes based on the presence of several species-specific signals, highlighting their inner genomic diversity. WCP with the
.
-derived Y (PSEMI-Y) probe painted not only the entire metacentric Y chromosome in males but also the X
and X
chromosomes in both male and female chromosomes of
In the cross-species experiments, the PSEMI-Y probe painted four acrocentric chromosomes in both males and females of the other tested
species. In summary, our results show that both intra- and interchromosomal rearrangements together with the dynamics of repetitive DNA significantly contributed to the karyotype divergence among
species, possibly promoted by specific populational and ecological traits and accompanied in one species by the origin of neo-sex chromosomes. The present results suggest how particular evolutionary scenarios found in fish species can help to clarify several issues related to genome organization and the karyotype evolution of vertebrates in general. |
|---|---|
| AbstractList | Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper the karyotype evolution of specific groups, especially the historically neglected small-sized ones. Representatives of the family Lebiasinidae (Characiformes) are a notable example, where only a few cytogenetic investigations have been conducted thus far. Here, we aim to elucidate the evolutionary processes behind the karyotype differentiation of
species on a finer-scale cytogenetic level. To achieve this, we applied C-banding, repetitive DNA mapping, CGH and WCP in
and
. Our results showed 2n = 42 in both sexes of
, while the difference in 2n between male and female in
(♂41/♀42) stands out due to the presence of a multiple X
X
Y sex chromosome system, until now undetected in this family. As a remarkable common feature, multiple 18S and 5S rDNA sites are present, with an occasional synteny or tandem-repeat amplification. Male-
.-female CGH experiments in
highlighted the accumulation of male-enriched repetitive sequences in the pericentromeric region of the Y chromosome. Inter-specific CGH experiments evidenced a divergence between both species' genomes based on the presence of several species-specific signals, highlighting their inner genomic diversity. WCP with the
.
-derived Y (PSEMI-Y) probe painted not only the entire metacentric Y chromosome in males but also the X
and X
chromosomes in both male and female chromosomes of
In the cross-species experiments, the PSEMI-Y probe painted four acrocentric chromosomes in both males and females of the other tested
species. In summary, our results show that both intra- and interchromosomal rearrangements together with the dynamics of repetitive DNA significantly contributed to the karyotype divergence among
species, possibly promoted by specific populational and ecological traits and accompanied in one species by the origin of neo-sex chromosomes. The present results suggest how particular evolutionary scenarios found in fish species can help to clarify several issues related to genome organization and the karyotype evolution of vertebrates in general. Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper the karyotype evolution of specific groups, especially the historically neglected small-sized ones. Representatives of the family Lebiasinidae (Characiformes) are a notable example, where only a few cytogenetic investigations have been conducted thus far. Here, we aim to elucidate the evolutionary processes behind the karyotype differentiation of Pyrrhulina species on a finer-scale cytogenetic level. To achieve this, we applied C-banding, repetitive DNA mapping, CGH and WCP in Pyrrhulina semifasciata and P. brevis. Our results showed 2n = 42 in both sexes of P. brevis, while the difference in 2n between male and female in P. semifasciata (♂41/♀42) stands out due to the presence of a multiple X1X2Y sex chromosome system, until now undetected in this family. As a remarkable common feature, multiple 18S and 5S rDNA sites are present, with an occasional synteny or tandem-repeat amplification. Male-vs.-female CGH experiments in P. semifasciata highlighted the accumulation of male-enriched repetitive sequences in the pericentromeric region of the Y chromosome. Inter-specific CGH experiments evidenced a divergence between both species’ genomes based on the presence of several species-specific signals, highlighting their inner genomic diversity. WCP with the P. semifasciata-derived Y (PSEMI-Y) probe painted not only the entire metacentric Y chromosome in males but also the X1 and X2 chromosomes in both male and female chromosomes of P. semifasciata. In the cross-species experiments, the PSEMI-Y probe painted four acrocentric chromosomes in both males and females of the other tested Pyrrhulina species. In summary, our results show that both intra- and interchromosomal rearrangements together with the dynamics of repetitive DNA significantly contributed to the karyotype divergence among Pyrrhulina species, possibly promoted by specific populational and ecological traits and accompanied in one species by the origin of neo-sex chromosomes. The present results suggest how particular evolutionary scenarios found in fish species can help to clarify several issues related to genome organization and the karyotype evolution of vertebrates in general. Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper the karyotype evolution of specific groups, especially the historically neglected small-sized ones. Representatives of the family Lebiasinidae (Characiformes) are a notable example, where only a few cytogenetic investigations have been conducted thus far. Here, we aim to elucidate the evolutionary processes behind the karyotype differentiation of Pyrrhulina species on a finer-scale cytogenetic level. To achieve this, we applied C-banding, repetitive DNA mapping, CGH and WCP in Pyrrhulina semifasciata and P. brevis. Our results showed 2n = 42 in both sexes of P. brevis, while the difference in 2n between male and female in P. semifasciata (♂41/♀42) stands out due to the presence of a multiple X1X2Y sex chromosome system, until now undetected in this family. As a remarkable common feature, multiple 18S and 5S rDNA sites are present, with an occasional synteny or tandem-repeat amplification. Male-vs.-female CGH experiments in P. semifasciata highlighted the accumulation of male-enriched repetitive sequences in the pericentromeric region of the Y chromosome. Inter-specific CGH experiments evidenced a divergence between both species' genomes based on the presence of several species-specific signals, highlighting their inner genomic diversity. WCP with the P. semifasciata-derived Y (PSEMI-Y) probe painted not only the entire metacentric Y chromosome in males but also the X1 and X2 chromosomes in both male and female chromosomes of P. semifasciata. In the cross-species experiments, the PSEMI-Y probe painted four acrocentric chromosomes in both males and females of the other tested Pyrrhulina species. In summary, our results show that both intra- and interchromosomal rearrangements together with the dynamics of repetitive DNA significantly contributed to the karyotype divergence among Pyrrhulina species, possibly promoted by specific populational and ecological traits and accompanied in one species by the origin of neo-sex chromosomes. The present results suggest how particular evolutionary scenarios found in fish species can help to clarify several issues related to genome organization and the karyotype evolution of vertebrates in general.Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper the karyotype evolution of specific groups, especially the historically neglected small-sized ones. Representatives of the family Lebiasinidae (Characiformes) are a notable example, where only a few cytogenetic investigations have been conducted thus far. Here, we aim to elucidate the evolutionary processes behind the karyotype differentiation of Pyrrhulina species on a finer-scale cytogenetic level. To achieve this, we applied C-banding, repetitive DNA mapping, CGH and WCP in Pyrrhulina semifasciata and P. brevis. Our results showed 2n = 42 in both sexes of P. brevis, while the difference in 2n between male and female in P. semifasciata (♂41/♀42) stands out due to the presence of a multiple X1X2Y sex chromosome system, until now undetected in this family. As a remarkable common feature, multiple 18S and 5S rDNA sites are present, with an occasional synteny or tandem-repeat amplification. Male-vs.-female CGH experiments in P. semifasciata highlighted the accumulation of male-enriched repetitive sequences in the pericentromeric region of the Y chromosome. Inter-specific CGH experiments evidenced a divergence between both species' genomes based on the presence of several species-specific signals, highlighting their inner genomic diversity. WCP with the P. semifasciata-derived Y (PSEMI-Y) probe painted not only the entire metacentric Y chromosome in males but also the X1 and X2 chromosomes in both male and female chromosomes of P. semifasciata. In the cross-species experiments, the PSEMI-Y probe painted four acrocentric chromosomes in both males and females of the other tested Pyrrhulina species. In summary, our results show that both intra- and interchromosomal rearrangements together with the dynamics of repetitive DNA significantly contributed to the karyotype divergence among Pyrrhulina species, possibly promoted by specific populational and ecological traits and accompanied in one species by the origin of neo-sex chromosomes. The present results suggest how particular evolutionary scenarios found in fish species can help to clarify several issues related to genome organization and the karyotype evolution of vertebrates in general. Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper the karyotype evolution of specific groups, especially the historically neglected small-sized ones. Representatives of the family Lebiasinidae (Characiformes) are a notable example, where only a few cytogenetic investigations have been conducted thus far. Here, we aim to elucidate the evolutionary processes behind the karyotype differentiation of Pyrrhulina species on a finer-scale cytogenetic level. To achieve this, we applied C-banding, repetitive DNA mapping, CGH and WCP in Pyrrhulina semifasciata and P. brevis . Our results showed 2n = 42 in both sexes of P. brevis , while the difference in 2n between male and female in P. semifasciata (♂41/♀42) stands out due to the presence of a multiple X 1 X 2 Y sex chromosome system, until now undetected in this family. As a remarkable common feature, multiple 18S and 5S rDNA sites are present, with an occasional synteny or tandem-repeat amplification. Male- vs .-female CGH experiments in P. semifasciata highlighted the accumulation of male-enriched repetitive sequences in the pericentromeric region of the Y chromosome. Inter-specific CGH experiments evidenced a divergence between both species’ genomes based on the presence of several species-specific signals, highlighting their inner genomic diversity. WCP with the P . semifasciata -derived Y (PSEMI-Y) probe painted not only the entire metacentric Y chromosome in males but also the X 1 and X 2 chromosomes in both male and female chromosomes of P. semifasciata. In the cross-species experiments, the PSEMI-Y probe painted four acrocentric chromosomes in both males and females of the other tested Pyrrhulina species. In summary, our results show that both intra- and interchromosomal rearrangements together with the dynamics of repetitive DNA significantly contributed to the karyotype divergence among Pyrrhulina species, possibly promoted by specific populational and ecological traits and accompanied in one species by the origin of neo-sex chromosomes. The present results suggest how particular evolutionary scenarios found in fish species can help to clarify several issues related to genome organization and the karyotype evolution of vertebrates in general. |
| Author | Hatanaka, Terumi Marinho, Manoela Maria Ferreira Cioffi, Marcelo de Bello Liehr, Thomas de Moraes, Renata Luiza Rosa Bertollo, Luiz Antônio Carlos Viana, Patrik F. Al-Rikabi, Ahmed B. H. Sember, Alexandr Feldberg, Eliana Ráb, Petr de Oliveira, Ezequiel Aguiar |
| AuthorAffiliation | 1 Laboratório de Citogenética de Peixes, Departamento de Genética e Evolução, Universidade Federal de São Carlos (UFSCar) , São Carlos , Brazil 3 Secretaria de Estado de Educação de Mato Grosso – SEDUC-MT , Cuiabá , Brazil 2 Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics, Czech Academy of Sciences , Liběchov , Czechia 6 Laboratório de Genética Animal, Instituto Nacional de Pesquisas da Amazônia, Coordenação de Biodiversidade , Manaus , Brazil 4 Museu de Zoologia da Universidade de São Paulo, (MZUSP) , São Paulo , Brazil 5 Institute of Human Genetics, University Hospital Jena , Jena , Germany |
| AuthorAffiliation_xml | – name: 6 Laboratório de Genética Animal, Instituto Nacional de Pesquisas da Amazônia, Coordenação de Biodiversidade , Manaus , Brazil – name: 1 Laboratório de Citogenética de Peixes, Departamento de Genética e Evolução, Universidade Federal de São Carlos (UFSCar) , São Carlos , Brazil – name: 2 Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics, Czech Academy of Sciences , Liběchov , Czechia – name: 4 Museu de Zoologia da Universidade de São Paulo, (MZUSP) , São Paulo , Brazil – name: 5 Institute of Human Genetics, University Hospital Jena , Jena , Germany – name: 3 Secretaria de Estado de Educação de Mato Grosso – SEDUC-MT , Cuiabá , Brazil |
| Author_xml | – sequence: 1 givenname: Renata Luiza Rosa surname: de Moraes fullname: de Moraes, Renata Luiza Rosa – sequence: 2 givenname: Alexandr surname: Sember fullname: Sember, Alexandr – sequence: 3 givenname: Luiz Antônio Carlos surname: Bertollo fullname: Bertollo, Luiz Antônio Carlos – sequence: 4 givenname: Ezequiel Aguiar surname: de Oliveira fullname: de Oliveira, Ezequiel Aguiar – sequence: 5 givenname: Petr surname: Ráb fullname: Ráb, Petr – sequence: 6 givenname: Terumi surname: Hatanaka fullname: Hatanaka, Terumi – sequence: 7 givenname: Manoela Maria Ferreira surname: Marinho fullname: Marinho, Manoela Maria Ferreira – sequence: 8 givenname: Thomas surname: Liehr fullname: Liehr, Thomas – sequence: 9 givenname: Ahmed B. H. surname: Al-Rikabi fullname: Al-Rikabi, Ahmed B. H. – sequence: 10 givenname: Eliana surname: Feldberg fullname: Feldberg, Eliana – sequence: 11 givenname: Patrik F. surname: Viana fullname: Viana, Patrik F. – sequence: 12 givenname: Marcelo de Bello surname: Cioffi fullname: Cioffi, Marcelo de Bello |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31428127$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright © 2019 de Moraes, Sember, Bertollo, de Oliveira, Ráb, Hatanaka, Marinho, Liehr, Al-Rikabi, Feldberg, Viana and Cioffi 2019 de Moraes, Sember, Bertollo, de Oliveira, Ráb, Hatanaka, Marinho, Liehr, Al-Rikabi, Feldberg, Viana and Cioffi |
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| Keywords | karyotype evolution comparative genomic hybridization (CGH) molecular cytogenetics sex chromosome chromosomal painting fishes |
| Language | English |
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| Title | Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae) |
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