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Neo-sex chromosomes of Ronderosia bergi: insight into the evolution of sex chromosomes in grasshoppers

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Abstract

Sex chromosomes have evolved many times from morphologically identical autosome pairs, most often presenting several recombination suppression events, followed by accumulation of repetitive DNA sequences. In Orthoptera, most species have an X0♂ sex chromosome system. However, in the subfamily Melanoplinae, derived variants of neo-sex chromosomes (neo-XY♂ or neo-X1X2Y♂) emerged several times. Here, we examined the differentiation of neo-sex chromosomes in a Melanoplinae species with a neo-XY♂/XX♀ system, Ronderosia bergi, using several approaches: (i) classical cytogenetic analysis, (ii) mapping via fluorescent in situ hybridization of some selected repetitive DNA sequences and microdissected sex chromosomes, and (iii) immunolocalization of distinct histone modifications. The microdissected sex chromosomes were also used as sources for Polymerase chain reaction (PCR) amplification of RNA-coding multigene families, to study variants related to the sex chromosomes. Our data suggest that the R. bergi neo-Y has become differentiated after its formation by a Robertsonian translocation and inversions, and has accumulated repetitive DNA sequences. Interestingly, the ex autosomes incorporated into the neo-sex chromosomes retain some autosomal post-translational histone modifications, at least in metaphase I, suggesting that the establishment of functional modifications in neo-sex chromosomes is slower than their sequence differentiation.

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Abbreviations

2n :

Diploid number

♀gDNA:

Female genomic DNA

BSA:

Bovine serum albumin

C 0 t-1 DNA:

C 0 is the initial concentration of single-stranded DNA in moles per liter and t is the reannealing time in seconds

DAPI:

4′,6-Diamidine-2′-phenylindole

FISH:

Fluorescence in situ hybridization

mya:

Million years ago

PBS:

Phosphate-buffered saline

PCR:

Polymerase chain reaction

Rb-translocation:

Robertsonian translocation

rDNA:

Ribosomal DNA

rRNA:

Ribosomal RNA

snRNA:

Small nuclear RNA

μX-DNA:

X chromosome DNA obtained by microdissection

μY-DNA:

Y chromosome DNA obtained by microdissection

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Acknowledgments

The authors are grateful to Frantisek Marec for critical reading of the manuscript and to the anonymous reviewers for their substantial contributions, and to “Parque Estadual Edmundo Navarro de Andrade” administration for sample collecting authorization. OMPG acknowledges scholarship obtained from Fundação de Amparo a Pesquisa do Estado de São Paulo-FAPESP (process number 2012/01421-7). This study was partly supported by FAPESP (process number 2014/11763-8), Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior-CAPES, Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq, and the Programa Primeiros Projetos-PROPE/UNESP from Brazil. DAM was supported by Consejo Nacional de Investigaciones Científicas y Técnicas-CONICET from Argentina. The authors are grateful to Antonio Sergio Pascon for technical assistance in obtaining embryos.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Departamento de Biologia, UNESP—Univ Estadual Paulista, Instituto de Biociências/IB, CEP 13506-900, Rio Claro, SP, Brazil

    O. M. Palacios-Gimenez & D. C. Cabral-de-Mello

  2. Laboratorio de Genética Evolutiva, IBS, Facultad de Ciencias Exactas, Químicas y Naturales, Universidad Nacional de Misiones, CONICET, 3300, Posadas, Argentina

    D. A. Marti

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  1. O. M. Palacios-Gimenez
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  2. D. A. Marti
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  3. D. C. Cabral-de-Mello
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Correspondence to D. C. Cabral-de-Mello.

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Supplementary material 1

FISH analysis for the C 0 t-1 and C 0 t-100 DNA fractions and three multigene families in the male mitotic metaphase complements of Ronderosia bergi. Each probe that was used and the neo-XY sex chromosome are indicated directly on the images. Note the absence of signals for multigene families in the sex chromosomes and the propagation of highly and moderately repetitive DNA sequences throughout the long arm of neo-Y chromosome; however, no differences in the distribution of the hybridization signals were observed with the distinct probes. Bar = 5 μm. (GIF 466 kb)

High resolution image (TIFF 6925 kb)

Supplementary material 2

FISH of the microsatellite probes in the male mitotic metaphase complements of Ronderosia bergi. Each probe that was used is indicated directly on the images. Note the specific and dispersed signals of the microsatellite arrays. The sex chromosomes are indicated. Bar = 5 μm. (GIF 509 kb)

High resolution image (TIFF 4247 kb)

Supplementary material 3

Alignment of the multigene family sequences that were isolated from the autosomes and sex chromosomes of Ronderosia bergi and Drosophila virilis. (GIF 169 kb)

High resolution image (TIFF 2404 kb)

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Palacios-Gimenez, O.M., Marti, D.A. & Cabral-de-Mello, D.C. Neo-sex chromosomes of Ronderosia bergi: insight into the evolution of sex chromosomes in grasshoppers. Chromosoma 124, 353–365 (2015). https://doi.org/10.1007/s00412-015-0505-1

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