Karyotypic stasis and its implications for extensive hybridization events in corallivores species of butterflyfishes (Chaetodontidae)

Wagner Franco Molina; Sudarat Khensuwan; Renata Luiza Rosa de Moraes; Francisco de Menezes Cavalcante Sassi; Gideão Wagner Werneck Félix da Costa; Davi Zalder Miguel; Weerayuth Supiwong; Sitthisak Jantarat; Krit Phintong; Kriengkrai Seetapan; Sukhonthip Ditcharoen; Alongklod Tanomtong; Thomas Liehr; Marcelo de Bello Cioffi

doi:10.1016/j.heliyon.2024.e27435

Karyotypic stasis and its implications for extensive hybridization events in corallivores species of butterflyfishes (Chaetodontidae)

Heliyon. 2024 Mar 5;10(6):e27435. doi: 10.1016/j.heliyon.2024.e27435. eCollection 2024 Mar 30.

Authors

Affiliations

¹ Department of Cell Biology and Genetics, Biosciences Center, Federal University of Rio Grande Do Norte, Natal, Brazil.
² Biology Program, Faculty of Science, Khon Kaen University, Muang, Khon Kaen, 40002, Thailand.
³ Department of Genetics and Evolution, Federal University of São Carlos, São Carlos, 13565-905, Brazil.
⁴ Faculty of Interdisciplinary Studies, Khon Kaen University. Nong Khai Campus, Muang, Nong Khai, 43000, Thailand.
⁵ Department of Science, Faculty of Science and Technology, Prince of Songkla University, Pattani, 94000, Thailand.
⁶ Department of Fundamental Science, Faculty of Science and Technology, Surindra Rajabhat University, Surin, Muang, 32000, Thailand.
⁷ School of Agriculture and Natural Resources, University of Phayao, Tumbol Maeka, Muang District, Phayao, 56000, Thailand.
⁸ Division of Biology, Faculty of Science and Technology, Rajamangala University of Technology Thanyaburi, Khlong Luang, Pathum Thani, 12110, Thailand.
⁹ Institut für Humangenetik, Universitätsklinikum Jena, Jena, 07747, Germany.

Abstract

The butterflyfishes (Chaetodontidae), emblematic inhabitants of coral reef environments, encompass the majority of known coralivorous species and show one of the highest hybridization rates known among vertebrates, making them an important evolutionary model. The vast knowledge about their life history and phylogenetic relationships contrasts with scarce information on their karyotype evolution. Aiming to expand the cytogenetic data of butterflyfishes and evaluate their karyotype evolution in association with evolutionary aspects, we conducted an extensive cytogenetic analysis in 20 species (Heniochus pleurotaenia and 19 Chaetodon spp.) from the Atlantic and Indo-Pacific regions, comparing the karyotype macrostructure and the arrangement of the 18S and 5S rDNA repetitive DNA classes in their chromosomes. The results demonstrate that butterflyfishes underwent a period of karyotypic stasis, as evidenced by their homoploid and structurally identical basal karyotype, which has 2n = 48 acrocentric chromosomes and is shared by 90% of species. Only C. trifascialis (2n = 48; FN = 50) and C. andamanensis (2n = 48; FN = 52) stood out because they both had karyotypes that diverged due to pericentric inversions. The microstructural arrays of 18S rDNA and 5S rDNA sequences were primarily comprised by single and independent loci on homologous chromosomes, indicating that there was little reshuffling among sets of orthologue chromosomes of species. Geographical comparisons revealed similar karyotypes between individuals of C. striatus from the Greater Caribbean and those of the coast of Brazil, corroborating previous data of gene flow through Amazon/Orinoco plume. The conservative chromosomal patterns in the butterflyfishes, likely overcome the limitations related to segregation and pairing of heterospecific complements and reinforce their contribution to the high degree of hybrid viability and introgression in Chaetodon species.

Keywords: Chromosomal conservatism; In situ hybridization; Percomorpha; rDNA.