Variations on a Theme: Genomics of Sex Determination in the Cichlid Fish Astatotilapia Burtoni

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2016 Nov 9

PMID 27821061

Citations 24

Authors

Astrid Bohne

Catherine A Wilson

John H Postlethwait

Walter Salzburger

Affiliations

Soon will be listed here.

Abstract

Background: Sex chromosomes change more frequently in fish than in mammals or birds. However, certain chromosomes or genes are repeatedly used as sex determinants in different members of the teleostean lineage. East African cichlids are an enigmatic model system in evolutionary biology representing some of the most diverse extant vertebrate adaptive radiations. How sex is determined and if different sex-determining mechanisms contribute to speciation is unknown for almost all of the over 1,500 cichlid species of the Great Lakes. Here, we investigated the genetic basis of sex determination in a cichlid from Lake Tanganyika, Astatotilapia burtoni, a member of the most species-rich cichlid lineage, the haplochromines.

Results: We used RAD-sequencing of crosses for two populations of A. burtoni, a lab strain and fish caught at the south of Lake Tanganyika. Using association mapping and comparative genomics, we confirmed male heterogamety in A. burtoni and identified different sex chromosomes (LG5 and LG18) in the two populations of the same species. LG5, the sex chromosome of the lab strain, is a fusion chromosome in A. burtoni. Wnt4 is located on this chromosome, representing the best candidate identified so far for the master sex-determining gene in our lab strain of A. burtoni.

Conclusions: Cichlids exemplify the high turnover rate of sex chromosomes in fish with two different chromosomes, LG5 and LG18, containing major sex-determining loci in the two populations of A. burtoni examined here. However, they also illustrate that particular chromosomes are more likely to be used as sex chromosomes. Chromosome 5 is such a chromosome, which has evolved several times as a sex chromosome, both in haplochromine cichlids from all Great Lakes and also in other teleost fishes.

Citing Articles

Diversity of Sex Chromosomes in Vertebrates: Six Novel Sex Chromosomes in Basal Haplochromines (Teleostei: Cichlidae).

Behrens K, Koblmueller S, Kocher T Genome Biol Evol. 2024; 16(7).

PMID: 39073759 PMC: 11285159. DOI: 10.1093/gbe/evae152.

Turnover of sex chromosomes in the Lake Tanganyika cichlid tribe Tropheini (Teleostei: Cichlidae).

Behrens K, Zimmermann H, Blazek R, Reichard M, Koblmuller S, Kocher T Sci Rep. 2024; 14(1):2471.

PMID: 38291228 PMC: 10828463. DOI: 10.1038/s41598-024-53021-3.

No evidence for sex chromosomes in natural populations of the cichlid fish Astatotilapia burtoni.

Lichilin N, Salzburger W, Bohne A G3 (Bethesda). 2023; 13(3).

PMID: 36649174 PMC: 9997565. DOI: 10.1093/g3journal/jkad011.

Characterization of sex chromosomes in three deeply diverged species of Pseudocrenilabrinae (Teleostei: Cichlidae).

Gammerdinger W, Conte M, Sandkam B, Penman D, Kocher T Hydrobiologia. 2022; 832(1):397-408.

PMID: 35665074 PMC: 9162429. DOI: 10.1007/s10750-018-3778-6.

New Sex Chromosomes in Lake Victoria Cichlid Fishes (Cichlidae: Haplochromini).

Kocher T, Behrens K, Conte M, Aibara M, Mrosso H, Green E Genes (Basel). 2022; 13(5).

PMID: 35627189 PMC: 9141883. DOI: 10.3390/genes13050804.

References

Smith D, Gordon I, Traut W, Herren J, Collins S, Martins D . A neo-W chromosome in a tropical butterfly links colour pattern, male-killing, and speciation. Proc Biol Sci. 2016; 283(1835). PMC: 4971206. DOI: 10.1098/rspb.2016.0821. View

Huffman L, OConnell L, Hofmann H . Aromatase regulates aggression in the African cichlid fish Astatotilapia burtoni. Physiol Behav. 2013; 112-113:77-83. DOI: 10.1016/j.physbeh.2013.02.004. View

Meyer A, Van de Peer Y . From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays. 2005; 27(9):937-45. DOI: 10.1002/bies.20293. View

Theis A, Salzburger W, Egger B . The function of anal fin egg-spots in the cichlid fish Astatotilapia burtoni. PLoS One. 2012; 7(1):e29878. PMC: 3252332. DOI: 10.1371/journal.pone.0029878. View

Kirkpatrick M, Guerrero R . Signatures of sex-antagonistic selection on recombining sex chromosomes. Genetics. 2014; 197(2):531-41. PMC: 4063913. DOI: 10.1534/genetics.113.156026. View

Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, Andrews J . Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science. 2003; 299(5607):697-700. PMC: 1363366. DOI: 10.1126/science.1079190. View

Ma Y, Zhang S, Xia Q, Zhang G, Huang X, Huang M . Molecular characterization of the TCP11 gene which is the human homologue of the mouse gene encoding the receptor of fertilization promoting peptide. Mol Hum Reprod. 2002; 8(1):24-31. DOI: 10.1093/molehr/8.1.24. View

Marshall Graves J, Peichel C . Are homologies in vertebrate sex determination due to shared ancestry or to limited options?. Genome Biol. 2010; 11(4):205. PMC: 2884537. DOI: 10.1186/gb-2010-11-4-205. View

Langmead B, Salzberg S . Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9(4):357-9. PMC: 3322381. DOI: 10.1038/nmeth.1923. View

10.

Robinson M, McCarthy D, Smyth G . edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009; 26(1):139-40. PMC: 2796818. DOI: 10.1093/bioinformatics/btp616. View

11.

Hattori R, Murai Y, Oura M, Masuda S, Majhi S, Sakamoto T . A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A. 2012; 109(8):2955-9. PMC: 3286941. DOI: 10.1073/pnas.1018392109. View

12.

Wang P, McCarrey J, Yang F, Page D . An abundance of X-linked genes expressed in spermatogonia. Nat Genet. 2001; 27(4):422-6. DOI: 10.1038/86927. View

13.

Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait J . Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics. 2011; 188(4):799-808. PMC: 3176089. DOI: 10.1534/genetics.111.127324. View

14.

Kaiser V, Ellegren H . Nonrandom distribution of genes with sex-biased expression in the chicken genome. Evolution. 2006; 60(9):1945-51. View

15.

Parnell N, Hulsey C, Streelman J . The genetic basis of a complex functional system. Evolution. 2012; 66(11):3352-66. PMC: 3490443. DOI: 10.1111/j.1558-5646.2012.01688.x. View

16.

Goodenough U, Heitman J . Origins of eukaryotic sexual reproduction. Cold Spring Harb Perspect Biol. 2014; 6(3). PMC: 3949356. DOI: 10.1101/cshperspect.a016154. View

17.

Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, Chaboissier M . Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol. 2006; 4(6):e187. PMC: 1463023. DOI: 10.1371/journal.pbio.0040187. View

18.

Perrin N . Sex reversal: a fountain of youth for sex chromosomes?. Evolution. 2009; 63(12):3043-9. DOI: 10.1111/j.1558-5646.2009.00837.x. View

19.

Bernard P, Harley V . Wnt4 action in gonadal development and sex determination. Int J Biochem Cell Biol. 2006; 39(1):31-43. DOI: 10.1016/j.biocel.2006.06.007. View

20.

Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M . B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genet. 2011; 7(8):e1002203. PMC: 3158035. DOI: 10.1371/journal.pgen.1002203. View