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Multiple karyotype differences between populations of the Hoplias malabaricus (Teleostei; Characiformes), a species complex in the gray area of the speciation process

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Abstract

Neotropical fishes exhibit remarkable karyotype diversity, whose evolution is poorly understood. Here, we studied genetic differences in 60 individuals, from 11 localities of one species, the wolf fish Hoplias malabaricus, from populations that include six different “karyomorphs”. These differ in Y-X chromosome differentiation, and, in several cases, by fusions with autosomes that have resulted in multiple sex chromosomes. Other differences are also observed in diploid chromosome numbers and morphologies. In an attempt to start understanding how this diversity was generated, we analyzed within- and between-population differences in a genome-wide sequence data set. We detect clear genotype differences between karyomorphs. Even in sympatry, samples with different karyomorphs differ more in sequence than samples from allopatric populations of the same karyomorph, suggesting that they represent populations that are to some degree reproductively isolated. However, sequence divergence between populations with different karyomorphs is remarkably low, suggesting that chromosome rearrangements may have evolved during a brief evolutionary time. We suggest that the karyotypic differences probably evolved in allopatry, in small populations that would have allowed rapid fixation of rearrangements, and that they became sympatric after their differentiation. Further studies are needed to test whether the karyotype differences contribute to reproductive isolation detected between some H. malabaricus karyomorphs.

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Fig. 1: Map of South America indicating the H. malabaricus localities analyzed.
Fig. 2: Population structure and genetic differentiation in H. malabaricus.

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Acknowledgements

MBC was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc. no 302449/2018-3) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Proc. 2023/00955-2). FHSS was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Proc. 2019/25009-7). MFP was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Proc. 2017/10240-0). TE was partially supported by an Australian Research Council Discovery Grant DP200101406 led by Erik Wapstra, Tariq Ezaz, Cristopher Burridge and Oleg Simakov. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001. This study was supported by INCT - Peixes, funded by MCTIC/CNPq (proc. 405706/2022-7). The authors declare no conflicts of interest. We thank Dr. Simon Martin (University of Edinburgh) for advice and assistance with analyses of population structure and introgression.

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Author notes

  1. These authors contributed equally: Fernando H. S. Souza, Manolo F. Perez.

  2. These authors jointly supervised this work: Deborah Charlesworth, Marcelo B. Cioffi.

Authors and Affiliations

  1. Laboratory of Evolutionary Cytogenetics, Department of Genetics and Evolution, Federal University of São Carlos, São Carlos, SP, Brazil

    Fernando H. S. Souza, Manolo F. Perez, Pedro H. N. Ferreira, Luiz A. C. Bertollo & Marcelo B. Cioffi

  2. Institute for Applied Ecology, University of Canberra, Canberra, NSW, Australia

    Tariq Ezaz

  3. Institute for Evolutionary Biology, Ashworth Laboratories, King’s Buildings, University of Edinburgh, Edinburgh, UK

    Deborah Charlesworth

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Contributions

FHSS, MFP, and MBC conceptualized the study. Sampling and formal analysis were executed by FHSS, MFP, DC, PHNF, and MBC. FHSS and MFP wrote the first draft of the manuscript with input from DC, LACB, and TE, and all authors contributed to subsequent revisions.

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Correspondence to Marcelo B. Cioffi.

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The authors declare no competing interests.

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Animals were collected with the authorization of the Brazilian environmental agency ICMBIO/SISBIO (license n°.48628-14) and SISGEN (A96FF09). Experiments followed ethical, and anesthesia conduct and were approved by the Ethics Committee on Animal Experimentation of the Universidade Federal de São Carlos (process number CEUA1853260315).

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Souza, F.H.S., Perez, M.F., Ferreira, P.H.N. et al. Multiple karyotype differences between populations of the Hoplias malabaricus (Teleostei; Characiformes), a species complex in the gray area of the speciation process. Heredity (2024). https://doi.org/10.1038/s41437-024-00707-z

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  • DOI: https://doi.org/10.1038/s41437-024-00707-z

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