Polygenic sex determination in the cichlid fish Astatotilapia burtoni

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Abstract

Background

The East African riverine cichlid species Astatotilapia burtoni serves as an important laboratory model for sexually dimorphic physiology and behavior, and also serves as an outgroup species for the explosive adaptive radiations of cichlid species in Lake Malawi and Lake Victoria. An astounding diversity of genetic sex determination systems have been revealed within the adaptive radiation of East African cichlids thus far, including polygenic sex determination systems involving the epistatic interaction of multiple, independently segregating sex determination alleles. However, sex determination has remained unmapped in A. burtoni. Here we present mapping results supporting the presence of multiple, novel sex determination alleles, and thus the presence of polygenic sex determination in A. burtoni.

Results

Using mapping in small families in conjunction with restriction-site associated DNA sequencing strategies, we identify associations with sex at loci on linkage group 13 and linkage group 5–14. Inheritance patterns support an XY sex determination system on linkage group 5–14 (a chromosome fusion relative to other cichlids studied), and an XYW system on linkage group 13, and these associations are replicated in multiple families. Additionally, combining our genetic data with comparative genomic analysis identifies another fusion that is unassociated with sex, with linkage group 8–24 and linkage group 16–21 fused in A. burtoni relative to other East African cichlid species.

Conclusions

We identify genetic signals supporting the presence of three previously unidentified sex determination alleles at two loci in the species A. burtoni, strongly supporting the presence of polygenic sex determination system in the species. These results provide a foundation for future mapping of multiple sex determination genes and their interactions. A better understanding of sex determination in A. burtoni provides important context for their use in behavioral studies, as well as studies of the evolution of genetic sex determination and sexual conflicts in East African cichlids.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-016-3177-1) contains supplementary material, which is available to authorized users.

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Most cited references 79

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The genomic substrate for adaptive radiation in African cichlid fish

David Brawand, Catherine E. Wagner, Yang I. Li … (2014)

Cichlid fishes are famous for large, diverse and replicated adaptive radiations in the Great Lakes of East Africa. To understand the molecular mechanisms underlying cichlid phenotypic diversity, we sequenced the genomes and transcriptomes of five lineages of African cichlids: the Nile tilapia (Oreochromis niloticus), an ancestral lineage with low diversity; and four members of the East African lineage: Neolamprologus brichardi/pulcher (older radiation, Lake Tanganyika), Metriaclima zebra (recent radiation, Lake Malawi), Pundamilia nyererei (very recent radiation, Lake Victoria), and Astatotilapia burtoni (riverine species around Lake Tanganyika). We found an excess of gene duplications in the East African lineage compared to tilapia and other teleosts, an abundance of non-coding element divergence, accelerated coding sequence evolution, expression divergence associated with transposable element insertions, and regulation by novel microRNAs. In addition, we analysed sequence data from sixty individuals representing six closely related species from Lake Victoria, and show genome-wide diversifying selection on coding and regulatory variants, some of which were recruited from ancient polymorphisms. We conclude that a number of molecular mechanisms shaped East African cichlid genomes, and that amassing of standing variation during periods of relaxed purifying selection may have been important in facilitating subsequent evolutionary diversification.

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Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle.

Songlin Chen, Guojie Zhang, Changwei Shao … (2014)

Genetic sex determination by W and Z chromosomes has developed independently in different groups of organisms. To better understand the evolution of sex chromosomes and the plasticity of sex-determination mechanisms, we sequenced the whole genomes of a male (ZZ) and a female (ZW) half-smooth tongue sole (Cynoglossus semilaevis). In addition to insights into adaptation to a benthic lifestyle, we find that the sex chromosomes of these fish are derived from the same ancestral vertebrate protochromosome as the avian W and Z chromosomes. Notably, the same gene on the Z chromosome, dmrt1, which is the male-determining gene in birds, showed convergent evolution of features that are compatible with a similar function in tongue sole. Comparison of the relatively young tongue sole sex chromosomes with those of mammals and birds identified events that occurred during the early phase of sex-chromosome evolution. Pertinent to the current debate about heterogametic sex-chromosome decay, we find that massive gene loss occurred in the wake of sex-chromosome 'birth'.

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The avian Z-linked gene DMRT1 is required for male sex determination in the chicken.

Craig A. Smith, Kelly Roeszler, Thomas Ohnesorg … (2009)

Sex in birds is chromosomally based, as in mammals, but the sex chromosomes are different and the mechanism of avian sex determination has been a long-standing mystery. In the chicken and all other birds, the homogametic sex is male (ZZ) and the heterogametic sex is female (ZW). Two hypotheses have been proposed for the mechanism of avian sex determination. The W (female) chromosome may carry a dominant-acting ovary determinant. Alternatively, the dosage of a Z-linked gene may mediate sex determination, two doses being required for male development (ZZ). A strong candidate avian sex-determinant under the dosage hypothesis is the conserved Z-linked gene, DMRT1 (doublesex and mab-3-related transcription factor 1). Here we used RNA interference (RNAi) to knock down DMRT1 in early chicken embryos. Reduction of DMRT1 protein expression in ovo leads to feminization of the embryonic gonads in genetically male (ZZ) embryos. Affected males show partial sex reversal, characterized by feminization of the gonads. The feminized left gonad shows female-like histology, disorganized testis cords and a decline in the testicular marker, SOX9. The ovarian marker, aromatase, is ectopically activated. The feminized right gonad shows a more variable loss of DMRT1 and ectopic aromatase activation, suggesting differential sensitivity to DMRT1 between left and right gonads. Germ cells also show a female pattern of distribution in the feminized male gonads. These results indicate that DMRT1 is required for testis determination in the chicken. Our data support the Z dosage hypothesis for avian sex determination.

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Author and article information

Contributors

Natalie B. Roberts: nbhodges@ncsu.edu

Scott A. Juntti: sjuntti@stanford.edu

Kaitlin P. Coyle: kate.coyle@ncsu.edu

Bethany L. Dumont: bldumont@ncsu.edu

M. Kaitlyn Stanley: mkstanle@ncsu.edu

Allyson Q. Ryan: allyson.ryan@embl.de

Russell D. Fernald: rfernald@stanford.edu

Reade B. Roberts: rbrober2@ncsu.edu

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 26 October 2016

Publication date PMC-release: 26 October 2016

Publication date Collection: 2016

Volume: 17

Electronic Location Identifier: 835

Affiliations

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

[2 ]Department of Biology, Stanford University, Stanford, CA USA

Article

Publisher ID: 3177

DOI: 10.1186/s12864-016-3177-1

PMC ID: 5080751

PubMed ID: 27784286

SO-VID: 90531a68-5c67-4de8-9b69-3f9c2d8b5e6c

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 15 June 2016

Date accepted : 18 October 2016

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000154, Division of Integrative Organismal Systems;

Award ID: 1456765

Award Recipient : Reade B. Roberts

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: NS034950

Award ID: NS093277

Award Recipient : Russell D. Fernald

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: sex determination,polygenic sex determination,cichlid,fish,evolution,astatotilapia burtoni

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ScienceOpen disciplines: Genetics

Keywords: sex determination, polygenic sex determination, cichlid, fish, evolution, astatotilapia burtoni

Polygenic sex determination in the cichlid fish Astatotilapia burtoni

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Behavioral Ecology of Fishes

Most cited references 79

The genomic substrate for adaptive radiation in African cichlid fish

Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle.

The avian Z-linked gene DMRT1 is required for male sex determination in the chicken.

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