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Sex chromosome evolution in frogs—helpful insights from chromosome painting in the genus Engystomops

Abstract

The differentiation of sex chromosomes is thought to be interrupted by relatively frequent sex chromosome turnover and/or occasional recombination between sex chromosomes (fountain-of-youth model) in some vertebrate groups as fishes, amphibians, and lizards. As a result, we observe the prevalence of homomorphic sex chromosomes in these groups. Here, we provide evidence for the loss of sex chromosome heteromorphism in the Amazonian frogs of the genus Engystomops, which harbors an intriguing history of sex chromosome evolution. In this species complex composed of two named species, two confirmed unnamed species, and up to three unconfirmed species, highly divergent karyotypes are present, and heteromorphic X and Y chromosomes were previously found in two species. We describe the karyotype of a lineage estimated to be the sister of all remaining Amazonian Engystomops (named Engystomops sp.) and perform chromosome painting techniques using one probe for the Y chromosome and one probe for the non-centromeric heterochromatic bands of the X chromosome of E. freibergi to compare three Engystomops karyotypes. The Y probe detected the Y chromosomes of E. freibergi and E. petersi and one homolog of chromosome pair 11 of Engystomops sp., suggesting their common evolutionary origin. The X probe showed no interspecific hybridization, revealing that X chromosome heterochromatin is strongly divergent among the studied species. In the light of the phylogenetic relationships, our data suggest that sex chromosome heteromorphism may have occurred early in the evolution of the Amazonian Engystomops and have been lost in two unnamed but confirmed candidate species.

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Fig. 1: Phylogenetic relationships of the Amazonian Engystomops inferred from mitochondrial (main image) and nuclear genes (inset) by Funk et al. (2012).
Fig. 2: Karyotype of Engystomops sp. from Amapá, Brazil.
Fig. 3: In situ hybridization of the pY and pXh probes.
Fig. 4: Cross species in situ hybridization of the pY probe.
Fig. 5: Ancestral reconstruction of sex chromosome conditions in the genus Engystomops.

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Acknowledgements

The authors are thankful for the access to equipment and assistance provided by the National Institute of Science and Technology on Photonics Applied to Cell Biology (INFABIC) at the State University of Campinas, the National Institute of Science and Technology on Ecology, Evolution and Biodiversity Conservation (INCT EECBio), and the Laboratory of Genetics and Biodiversity, both at the Federal University of Goiás. The authors thank Janaína Reis Ferreira Lima for her help with field collection. LBL thanks Dr Antonio Baca Sánchez for his important help in the initial assays of chromosome microdissection. This study had the financial support of Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP #2009/02405-2; #2008/11326-6) and Fundo de apoio ao ensino, pesquisa e extensão da Unicamp (FAEPEX #519292/435/11).

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Targueta, C.P., Krylov, V., Nondilo, T.E. et al. Sex chromosome evolution in frogs—helpful insights from chromosome painting in the genus Engystomops. Heredity 126, 396–409 (2021). https://doi.org/10.1038/s41437-020-00385-7

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