Dual control by a single gene of secondary sexual characters and mating preferences in medaka.

Shoji Fukamachi, Masato Kinoshita, Kouichi Aizawa, Shoji Oda, Axel Meyer, Hiroshi Mitani
Author Information
  1. Shoji Fukamachi: Department of Biology, University of Konstanz, D-78457 Konstanz, Germany. fukasho@hotmail.com

Abstract

BACKGROUND: Animals utilize a wide variety of tactics to attract reproductive partners. Behavioral experiments often indicate an important role for visual cues in fish, but their molecular basis remains almost entirely unknown. Studies on model species (such as zebrafish and medaka) allow investigations into this fundamental question in behavioral and evolutionary biology.
RESULTS: Through mate-choice experiences using several laboratory strains of various body colors, we successfully identified one medaka mutant (color interfere; ci) that is distinctly unattractive to reproductive partners. This unattractiveness seems to be due to reduced orange pigment cells (xanthophores) in the skin. The ci strain carries a mutation on the somatolactin alpha (SLa) gene, therefore we expected over-expression of SLa to make medaka hyper-attractive. Indeed, extremely strong mating preferences were detected in a choice between the ci and SLa-transgenic (Actb-SLa:GFP) medaka. Intriguingly, however, the strains showed opposite biases; that is, the mutant and transgenic medaka liked to mate with partners from their own strain, similar to becoming sexually isolated.
CONCLUSION: This study spotlighted SLa as a novel mate-choice gene in fish. In addition, these results are the first demonstration of a single gene that can pleiotropically and harmoniously change both secondary sexual characters and mating preferences. Although theoretical models have long suggested joint evolution of linked genes on a chromosome, a mutation on a gene-regulatory region (that is, switching on/off of a single gene) might be sufficient to trigger two 'runaway' processes in different directions to promote (sympatric) speciation.

References

  1. J Evol Biol. 2008 Nov;21(6):1452-9 [PMID: 18823452]
  2. Trends Ecol Evol. 2006 Jun;21(6):296-302 [PMID: 16769428]
  3. Adv Genet. 2007;59:147-71 [PMID: 17888798]
  4. Nature. 2009 Feb 19;457(7232):1007-11 [PMID: 19098895]
  5. Genetics. 2004 Nov;168(3):1519-27 [PMID: 15579703]
  6. Nature. 2008 Aug 28;454(7208):1115-8 [PMID: 18650807]
  7. Dev Genes Evol. 2006 Mar;216(3):152-7 [PMID: 16344968]
  8. Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10661-6 [PMID: 15249680]
  9. Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14628-31 [PMID: 8962104]
  10. Nature. 2008 Oct 2;455(7213):620-6 [PMID: 18833272]
  11. Gene. 2006 Apr 26;371(2):268-78 [PMID: 16460888]
  12. Gene. 2009 Aug 1;442(1-2):81-7 [PMID: 19393303]
  13. Heredity (Edinb). 2009 Jan;102(1):39-44 [PMID: 18648383]
  14. J Mol Evol. 2007 Oct;65(4):359-72 [PMID: 17917757]
  15. J Exp Zool A Comp Exp Biol. 2006 Oct 1;305(10):890-6 [PMID: 16941651]
  16. Genetics. 2005 Dec;171(4):1875-83 [PMID: 16143602]
  17. Proc Biol Sci. 2006 Feb 7;273(1584):257-66 [PMID: 16543167]
  18. PLoS Biol. 2005 Sep;3(9):e282 [PMID: 16149849]
  19. Zebrafish. 2008 Dec;5(4):297-307 [PMID: 19133828]
  20. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3721-5 [PMID: 16593036]
  21. Anim Behav. 1998 May;55(5):1151-63 [PMID: 9632501]
  22. J Endocrinol. 1992 Jun;133(3):393-403 [PMID: 1613440]
  23. Biol Lett. 2009 Apr 23;5(2):225-8 [PMID: 19033131]
  24. Development. 2001 Oct;128(20):4035-44 [PMID: 11641226]
  25. Science. 2008 Nov 7;322(5903):904-9 [PMID: 18988843]
  26. Proc Biol Sci. 1995 Mar 22;259(1356):307-11 [PMID: 7740048]
  27. Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2934-8 [PMID: 14976259]
  28. Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9737-42 [PMID: 19487670]
  29. Nat Genet. 2001 Aug;28(4):381-5 [PMID: 11479596]
  30. Trends Ecol Evol. 2004 May;19(5):264-71 [PMID: 16701266]
  31. Reprod Biol Endocrinol. 2008 Sep 15;6:42 [PMID: 18793397]
  32. Embryologia (Nagoya). 1965 Feb;9:299-307 [PMID: 14346503]
  33. Proc Biol Sci. 2005 Feb 7;272(1560):303-9 [PMID: 15705556]
  34. Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6575-80 [PMID: 16611733]

MeSH Term

Animals
Animals, Genetically Modified
Cues
Female
Fish Proteins
Male
Mating Preference, Animal
Mutation
Oryzias
Sex Characteristics

Chemicals

Fish Proteins

Word Cloud

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