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Genetic sex determination in Astatotilapia calliptera, a prototype species for the Lake Malawi cichlid radiation

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Abstract

East African cichlids display extensive variation in sex determination systems. The species Astatotilapia calliptera is one of the few cichlids that reside both in Lake Malawi and in surrounding waterways. A. calliptera is of interest in evolutionary studies as a putative immediate outgroup species for the Lake Malawi species flock and possibly as a prototype ancestor-like species for the radiation. Here, we use linkage mapping to test association of sex in A. calliptera with loci that have been previously associated with genetic sex determination in East African cichlid species. We identify a male heterogametic XY system segregating at linkage group (LG) 7 in an A. calliptera line that originated from Lake Malawi, at a locus previously shown to act as an XY sex determination system in multiple species of Lake Malawi cichlids. Significant association of genetic markers and sex produce a broad genetic interval of approximately 26 megabases (Mb) using the Nile tilapia genome to orient markers; however, we note that the marker with the strongest association with sex is near a gene that acts as a master sex determiner in other fish species. We demonstrate that alleles of the marker are perfectly associated with sex in Metriaclima mbenjii, a species from the rock-dwelling clade of Lake Malawi. While we do not rule out the possibility of other sex determination loci in A. calliptera, this study provides a foundation for fine mapping of the cichlid sex determination gene on LG7 and evolutionary context regarding the origin and persistence of the LG7 XY across diverse, rapidly evolving lineages.

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Acknowledgements

We thank Kaitlyn Stanley for the technical support, Adam Miranda for the aquaculture support, and Patrick Ciccotto for the valuable insight during manuscript preparation. The work was funded by support to RBR from the National Science Foundation (Grant IOS-1456765).

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Authors and Affiliations

  1. Department of Biological Sciences and W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, USA

    Erin N. Peterson, Maggie E. Cline, Emily C. Moore, Natalie B. Roberts & Reade B. Roberts

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  1. Erin N. Peterson
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  2. Maggie E. Cline
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  3. Emily C. Moore
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  4. Natalie B. Roberts
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  5. Reade B. Roberts
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Correspondence to Reade B. Roberts.

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Research involving human participants and/or animals

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted, specifically under the approval and oversight of the Institutional Animal Care and Use Committee at North Carolina State University (protocol 15-043-O).

This article does not contain any studies with human participants performed by any of the authors.

Additional information

Communicated by: Sven Thatje

Electronic supplementary material

Online resource 1

Primer sequences for SSR markers used in study, including location of markers by A. burtoni scaffold and O. niloticus linkage group. (PDF 86 kb)

Online resource 2

Spreadsheet of marker genotype data. Genotypes are provided as numerical allele sizes and color-coded based on parental haplotypes manually inferred from inheritance patterns (dam haplotypes, pink; sire haplotypes, blue; non-informative, no color). Each row provides the genotype information for one individual, with markers ordered per their comparative location on the O. niloticus genome. Data is grouped separately by family, with parental haplotypes at the top of each. (XLSX 50 kb)

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Peterson, E.N., Cline, M.E., Moore, E.C. et al. Genetic sex determination in Astatotilapia calliptera, a prototype species for the Lake Malawi cichlid radiation. Sci Nat 104, 41 (2017). https://doi.org/10.1007/s00114-017-1462-8

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