Genome biology of the darkedged splitfin, Girardinichthys multiradiatus, and the evolution of sex chromosomes and placentation
- Kang Du1,
- Martin Pippel2,
- Susanne Kneitz3,
- Romain Feron4,5,
- Irene da Cruz6,
- Sylke Winkler2,
- Brigitta Wilde3,
- Edgar G. Avila Luna7,
- Gene Myers2,8,
- Yann Guiguen5,8,
- Constantino Macias Garcia7,8 and
- Manfred Schartl1,5
- 1The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry, Texas State University, San Marcos, Texas 78666, USA;
- 2Max-Planck Institute of Molecular Cell Biology and Genetics, 10307 Dresden, Germany;
- 3Biochemistry and Cell Biology, Biocenter, University of Wuerzburg, 97074 Wuerzburg, Germany;
- 4Department of Ecology and Evolution, University of Lausanne, and Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland;
- 5INRAE, LPGP, 35000 Rennes, France;
- 6Developmental Biochemistry, Biocenter, University of Wuerzburg, 97074 Wuerzburg, Germany;
- 7Instituto de Ecologia, Universidad Nacional Autónoma de México, C.P. 04510, Mexico City D.F., Mexico
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↵8 These authors are co-senior authors and contributed equally to this work.
Abstract
Viviparity evolved independently about 150 times in vertebrates and more than 20 times in fish. Several lineages added to the protection of the embryo inside the body of the mother, the provisioning of nutrients, and physiological exchange. This often led to the evolution of a placenta. Among fish, one of the most complex systems serving the function of the placenta is the embryonal trophotaenia/ovarian luminal epithelium of the goodeid fishes. For a better understanding of this feature and others of this group of fishes, high-quality genomic resources are essential. We have sequenced the genome of the darkedged splitfin, Girardinichthys multiradiatus. The assembly is chromosome level and includes the X and Y Chromosomes. A large male-specific region on the Y was identified covering 80% of Chromosome 20, allowing some first inferences on the recent origin and a candidate male sex determining gene. Genome-wide transcriptomics uncovered sex-specific differences in brain gene expression with an enrichment for neurosteroidogenesis and testis genes in males. The expression signatures of the splitfin embryonal and maternal placenta showed overlap with homologous tissues including human placenta, the ovarian follicle epithelium of matrotrophic poeciliid fish species and the brood pouch epithelium of the seahorse. Our comparative analyses on the evolution of embryonal and maternal placenta indicate that the evolutionary novelty of maternal provisioning development repeatedly made use of genes that already had the same function in other tissues. In this way, preexisting modules are assembled and repurposed to provide the molecular changes for this novel trait.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.275826.121.
- Received May 28, 2021.
- Accepted January 10, 2022.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
