Persistence of Mhc heterozygosity in homozygous clonal killifish, Rivulus marmoratus: Implications for the origin of hermaphroditism

Akie Sato, Yoko Satta, Felipe Figueroa, Werner E. Mayer, Zofia Zaleska-Rutczynska, Satoru Toyosawa, Joseph Travis, Jan Klein

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

The mangrove killifish Rivulus marmoratus, a neotropical fish in the order Cyprinodontiformes, is the only known obligatorily selfing, synchronous hermaphroditic vertebrate. To shed light on its population structure and the origin of hermaphroditism, major histocompatibility complex (Mhc) class I genes of the killifish from seven different localities in Florida, Belize, and the Bahamas were cloned and sequenced. Thirteen loci and their alleles were identified and classified into eight groups. The loci apparently arose ∼20 million years ago (MYA) by gene duplications from a single common progenitor in the ancestors of R. marmoratus and its closest relatives. Distinct loci were found to be restricted to different populations and different individuals in the same population. Up to 44% of the fish were heterozygotes at Mhc loci, as compared to near homozygosity non-Mhc loci. Large genetic distances between some of the Mhc alleles revealed the presence of ancestral allelic lineages. Computer simulation designed to explain these findings indicated that selfing is incomplete in R. marmoratus populations, that Mhc allelic lineages must have diverged before the onset of selfing, and that the hermaphroditism arose in a population containing multiple ancestral Mhc lineages. A model is proposed in which hermaphroditism arose stage-wise by mutations, each of which spread through the entire population and was fixed independently in the emerging clones.

Original languageEnglish (US)
Pages (from-to)1791-1803
Number of pages13
JournalGenetics
Volume162
Issue number4
StatePublished - Dec 1 2002

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Fundulidae
Disorders of Sex Development
Major Histocompatibility Complex
Population
Fishes
Bahamas
Belize
Alleles
Cyprinodontiformes
MHC Class I Genes
Gene Duplication
Heterozygote
Computer Simulation
Vertebrates
Clone Cells
Mutation

All Science Journal Classification (ASJC) codes

  • Genetics

Cite this

Sato, A., Satta, Y., Figueroa, F., Mayer, W. E., Zaleska-Rutczynska, Z., Toyosawa, S., ... Klein, J. (2002). Persistence of Mhc heterozygosity in homozygous clonal killifish, Rivulus marmoratus: Implications for the origin of hermaphroditism. Genetics, 162(4), 1791-1803.
Sato, Akie ; Satta, Yoko ; Figueroa, Felipe ; Mayer, Werner E. ; Zaleska-Rutczynska, Zofia ; Toyosawa, Satoru ; Travis, Joseph ; Klein, Jan. / Persistence of Mhc heterozygosity in homozygous clonal killifish, Rivulus marmoratus : Implications for the origin of hermaphroditism. In: Genetics. 2002 ; Vol. 162, No. 4. pp. 1791-1803.
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Sato, A, Satta, Y, Figueroa, F, Mayer, WE, Zaleska-Rutczynska, Z, Toyosawa, S, Travis, J & Klein, J 2002, 'Persistence of Mhc heterozygosity in homozygous clonal killifish, Rivulus marmoratus: Implications for the origin of hermaphroditism', Genetics, vol. 162, no. 4, pp. 1791-1803.

Persistence of Mhc heterozygosity in homozygous clonal killifish, Rivulus marmoratus : Implications for the origin of hermaphroditism. / Sato, Akie; Satta, Yoko; Figueroa, Felipe; Mayer, Werner E.; Zaleska-Rutczynska, Zofia; Toyosawa, Satoru; Travis, Joseph; Klein, Jan.

In: Genetics, Vol. 162, No. 4, 01.12.2002, p. 1791-1803.

Research output: Contribution to journalArticle

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AU - Sato, Akie

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N2 - The mangrove killifish Rivulus marmoratus, a neotropical fish in the order Cyprinodontiformes, is the only known obligatorily selfing, synchronous hermaphroditic vertebrate. To shed light on its population structure and the origin of hermaphroditism, major histocompatibility complex (Mhc) class I genes of the killifish from seven different localities in Florida, Belize, and the Bahamas were cloned and sequenced. Thirteen loci and their alleles were identified and classified into eight groups. The loci apparently arose ∼20 million years ago (MYA) by gene duplications from a single common progenitor in the ancestors of R. marmoratus and its closest relatives. Distinct loci were found to be restricted to different populations and different individuals in the same population. Up to 44% of the fish were heterozygotes at Mhc loci, as compared to near homozygosity non-Mhc loci. Large genetic distances between some of the Mhc alleles revealed the presence of ancestral allelic lineages. Computer simulation designed to explain these findings indicated that selfing is incomplete in R. marmoratus populations, that Mhc allelic lineages must have diverged before the onset of selfing, and that the hermaphroditism arose in a population containing multiple ancestral Mhc lineages. A model is proposed in which hermaphroditism arose stage-wise by mutations, each of which spread through the entire population and was fixed independently in the emerging clones.

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Sato A, Satta Y, Figueroa F, Mayer WE, Zaleska-Rutczynska Z, Toyosawa S et al. Persistence of Mhc heterozygosity in homozygous clonal killifish, Rivulus marmoratus: Implications for the origin of hermaphroditism. Genetics. 2002 Dec 1;162(4):1791-1803.