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Satellitome analysis on the pale-breasted thrush Turdus leucomelas (Passeriformes; Turdidae) uncovers the putative co-evolution of sex chromosomes and satellite DNAs

Do all birds' sex chromosomes follow the same canonical one-way direction of evolution? We combined cytogenetic and genomic approaches to analyze the process of the W chromosomal differentiation in two selected Passeriform species, named the Pale-breasted Thrush Turdus leucomelas and the Rufous...

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Published in:Scientific reports 2024-09, Vol.14 (1), p.20656-14, Article 20656
Main Authors: Souza, Guilherme Mota, Kretschmer, Rafael, Toma, Gustavo Akira, de Oliveira, Alan Moura, Deon, Geize Aparecida, Setti, Princia Grejo, Zeni dos Santos, Rodrigo, Goes, Caio Augusto Gomes, Del Valle Garnero, Analía, Gunski, Ricardo José, de Oliveira, Edivaldo Herculano Correa, Porto-Foresti, Fabio, Liehr, Thomas, Utsunomia, Ricardo, de Bello Cioffi, Marcelo
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creator Souza, Guilherme Mota
Kretschmer, Rafael
Toma, Gustavo Akira
de Oliveira, Alan Moura
Deon, Geize Aparecida
Setti, Princia Grejo
Zeni dos Santos, Rodrigo
Goes, Caio Augusto Gomes
Del Valle Garnero, Analía
Gunski, Ricardo José
de Oliveira, Edivaldo Herculano Correa
Porto-Foresti, Fabio
Liehr, Thomas
Utsunomia, Ricardo
de Bello Cioffi, Marcelo
description Do all birds' sex chromosomes follow the same canonical one-way direction of evolution? We combined cytogenetic and genomic approaches to analyze the process of the W chromosomal differentiation in two selected Passeriform species, named the Pale-breasted Thrush Turdus leucomelas and the Rufous-bellied thrush T. rufiventris . We characterized the full catalog of satellite DNAs (satellitome) of T. leucomelas , and the 10 TleSatDNA classes obtained together with 16 microsatellite motifs were in situ mapped in both species. Additionally, using Comparative Genomic Hybridization (CGH) assays, we investigated their intragenomic variations. The W chromosomes of both species did not accumulate higher amounts of both heterochromatin and repetitive sequences. However, while T. leucomelas showed a heterochromatin-poor W chromosome with a very complex evolutionary history, T. rufiventris showed a small and partially heterochromatic W chromosome that represents a differentiated version of its original autosomal complement (Z chromosome). The combined approach of CGH and sequential satDNA mapping suggest the occurrence of a former W-autosomal translocation event in T. leucomelas , which had an impact on the W chromosome in terms of sequence gains and losses. At the same time, an autosome, which is present in both males and females in a polymorphic state, lost sequences and integrated previously W-specific ones. This putative W-autosomal translocation, however, did not result in the emergence of a multiple-sex chromosome system. Instead, the generation of a neo-W chromosome suggests an unexpected evolutionary trajectory that deviates from the standard canonical model of sex chromosome evolution.
doi_str_mv 10.1038/s41598-024-71635-5
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We combined cytogenetic and genomic approaches to analyze the process of the W chromosomal differentiation in two selected Passeriform species, named the Pale-breasted Thrush Turdus leucomelas and the Rufous-bellied thrush T. rufiventris . We characterized the full catalog of satellite DNAs (satellitome) of T. leucomelas , and the 10 TleSatDNA classes obtained together with 16 microsatellite motifs were in situ mapped in both species. Additionally, using Comparative Genomic Hybridization (CGH) assays, we investigated their intragenomic variations. The W chromosomes of both species did not accumulate higher amounts of both heterochromatin and repetitive sequences. However, while T. leucomelas showed a heterochromatin-poor W chromosome with a very complex evolutionary history, T. rufiventris showed a small and partially heterochromatic W chromosome that represents a differentiated version of its original autosomal complement (Z chromosome). 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Turdidae) uncovers the putative co-evolution of sex chromosomes and satellite DNAs</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2024-09-04</date><risdate>2024</risdate><volume>14</volume><issue>1</issue><spage>20656</spage><epage>14</epage><pages>20656-14</pages><artnum>20656</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Do all birds' sex chromosomes follow the same canonical one-way direction of evolution? We combined cytogenetic and genomic approaches to analyze the process of the W chromosomal differentiation in two selected Passeriform species, named the Pale-breasted Thrush Turdus leucomelas and the Rufous-bellied thrush T. rufiventris . We characterized the full catalog of satellite DNAs (satellitome) of T. leucomelas , and the 10 TleSatDNA classes obtained together with 16 microsatellite motifs were in situ mapped in both species. Additionally, using Comparative Genomic Hybridization (CGH) assays, we investigated their intragenomic variations. The W chromosomes of both species did not accumulate higher amounts of both heterochromatin and repetitive sequences. However, while T. leucomelas showed a heterochromatin-poor W chromosome with a very complex evolutionary history, T. rufiventris showed a small and partially heterochromatic W chromosome that represents a differentiated version of its original autosomal complement (Z chromosome). The combined approach of CGH and sequential satDNA mapping suggest the occurrence of a former W-autosomal translocation event in T. leucomelas , which had an impact on the W chromosome in terms of sequence gains and losses. At the same time, an autosome, which is present in both males and females in a polymorphic state, lost sequences and integrated previously W-specific ones. This putative W-autosomal translocation, however, did not result in the emergence of a multiple-sex chromosome system. Instead, the generation of a neo-W chromosome suggests an unexpected evolutionary trajectory that deviates from the standard canonical model of sex chromosome evolution.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>39232109</pmid><doi>10.1038/s41598-024-71635-5</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record>
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subjects 631/208/1405
631/208/182
631/208/212
Animals
Chromosomes
Coevolution
Comparative Genomic Hybridization
Cytogenetics
DNA, Satellite - genetics
Evolution
Evolution, Molecular
Evolutionary genetics
Female
Gene mapping
Genomics
Heterochromatin
Heterochromatin - genetics
Humanities and Social Sciences
Hybridization
In Situ Hybridization, Fluorescence
Male
Microsatellite Repeats - genetics
Molecular cytogenetics
multidisciplinary
Neo sex chromosomes
Passeriformes - genetics
satDNA
Science
Science (multidisciplinary)
Sex chromosomes
Sex Chromosomes - genetics
Translocation
Turdus leucomelas
W chromosomes
Z chromosomes
title Satellitome analysis on the pale-breasted thrush Turdus leucomelas (Passeriformes; Turdidae) uncovers the putative co-evolution of sex chromosomes and satellite DNAs
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