TY - JOUR

T1 - Whole-chromosome fusions in the karyotype evolution of Sceloporus (Iguania, Reptilia) are more frequent in sex chromosomes than autosomes

AU - Lisachov, Artem P.

AU - Tishakova, Katerina V.

AU - Romanenko, Svetlana A.

AU - Molodtseva, Anna S.

AU - Prokopov, Dmitry Yu

AU - Pereira, Jorge C.

AU - Ferguson-Smith, Malcolm A.

AU - Borodin, Pavel M.

AU - Trifonov, Vladimir A.

N1 - Funding Information: Ethics. All manipulations with animals were approved by the Institute of Molecular and Cellular Biology Ethics Committee (statement no. 01/18 from 5 March 2018). Data accessibility. The NGS data were deposited in NCBI SRA database under the accession no. PRJNA616430. Authors’ contributions. A.P.L. performed the synaptonemal complex analysis and DNA barcoding. K.V.T. performed FISH. S.A.R. performed cell culturing. A.S.M. prepared the Illumina DNA libraries. D.Y.P. performed bioinformatic analysis. J.C.P. and M.A.F.-S. obtained the flow-sorted chromosome-specific probes. A.P.L., V.A.T. and P.M.B. designed the study. All authors participated in writing and editing the manuscript, gave final approval for publication and agree to be held accountable for the work performed therein. Competing interests. We declare we have no competing interests. Funding. This work was supported by the research grant no. 19-54-26017 from the Russian Foundation for Basic Research, the research grant no. 2019-0546 (FSUS-2020-0040) and no. 0324-2019-0042 from the Ministry of Science and Higher Education (Russia) via the Novosibirsk State University and the Institute of Cytology and Genetics. Acknowledgements. We thank the Microscopic Center of the Siberian Branch of the Russian Academy of Sciences for granting access to microscopic equipment. We thank I. Kichigin for help in NGS data analysis and K. Petrova for assisting in G-banding of S. malachiticus chromosomes. Publisher Copyright: © 2021 The Author(s).

PY - 2021/9/13

Y1 - 2021/9/13

N2 - Whole-chromosome fusions play a major role in the karyotypic evolution of reptiles. It has been suggested that certain chromosomes tend to fuse with sex chromosomes more frequently than others. However, the comparative genomic synteny data are too scarce to draw strong conclusions. We obtained and sequenced chromosome-specific DNA pools of Sceloporus malachiticus, an iguanian species which has experienced many chromosome fusions. We found that four of seven lineage-specific fusions involved sex chromosomes, and that certain syntenic blocks which constitute the sex chromosomes, such as the homologues of the Anolis carolinensis chromosomes 11 and 16, are repeatedly involved in sex chromosome formation in different squamate species. To test the hypothesis that the karyotypic shift could be associated with changes in recombination patterns, we performed a synaptonemal complex analysis in this species and in Sceloporus variabilis (2n = 34). It revealed that the sex chromosomes in S. malachiticus had two distal pseudoautosomal regions and a medial differentiated region. We found that multiple fusions little affected the recombination rate in S. malachiticus. Our data confirm more frequent involvement of certain chromosomes in sex chromosome formation, but do not reveal a connection between the gonosome-autosome fusions and the evolution of recombination rate. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.

AB - Whole-chromosome fusions play a major role in the karyotypic evolution of reptiles. It has been suggested that certain chromosomes tend to fuse with sex chromosomes more frequently than others. However, the comparative genomic synteny data are too scarce to draw strong conclusions. We obtained and sequenced chromosome-specific DNA pools of Sceloporus malachiticus, an iguanian species which has experienced many chromosome fusions. We found that four of seven lineage-specific fusions involved sex chromosomes, and that certain syntenic blocks which constitute the sex chromosomes, such as the homologues of the Anolis carolinensis chromosomes 11 and 16, are repeatedly involved in sex chromosome formation in different squamate species. To test the hypothesis that the karyotypic shift could be associated with changes in recombination patterns, we performed a synaptonemal complex analysis in this species and in Sceloporus variabilis (2n = 34). It revealed that the sex chromosomes in S. malachiticus had two distal pseudoautosomal regions and a medial differentiated region. We found that multiple fusions little affected the recombination rate in S. malachiticus. Our data confirm more frequent involvement of certain chromosomes in sex chromosome formation, but do not reveal a connection between the gonosome-autosome fusions and the evolution of recombination rate. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.

KW - FISH

KW - flow-sorted chromosome probes

KW - lizards

KW - next-generation sequencing

KW - synaptonemal complexes

KW - Biological Evolution

KW - Lizards/genetics

KW - Synaptonemal Complex/genetics

KW - Animals

KW - Male

KW - Karyotype

KW - Sex Chromosomes/genetics

UR - http://www.scopus.com/inward/record.url?scp=85111084717&partnerID=8YFLogxK

U2 - 10.1098/rstb.2020.0099

DO - 10.1098/rstb.2020.0099

M3 - Article

C2 - 34304596

AN - SCOPUS:85111084717

VL - 376

JO - Philosophical Transactions of the Royal Society B: Biological Sciences

JF - Philosophical Transactions of the Royal Society B: Biological Sciences

SN - 0800-4622

IS - 1833

M1 - 20200099

ER -