OMIA 001890-198806 : Male body size/courtship behaviour in Philomachus pugnax

In other species: Panuco swordtail , Perugia's limia

Mendelian trait/disorder: yes

Mode of inheritance: Autosomal

Considered a defect: no

Key variant known: yes

Year key variant first reported: 2015

Species-specific description: Lank et al. (1995) described two "morphs" in this species: independent males "have a territorial breeding strategy of defending lek mating courts against other independents" while satellites, which are non-territorial, "move among, are recruited to and share independents' courts". Jukema and Piersma (2006) added a third, namely "faeder": "Faeders are slightly larger than females and in late April have testes 2.5 time the size of testes of normal males. On leks in aviaries and in the wild they appear to combine feminine and masculine behaviours. Faeders may represent the ancestral, care-giving, male strategy, but their relatively large testes suggest that currently they behave as sneakers."

A video demonstrating ruff male reproductive strategies at a lek in Karesuando, Sweden is viewable at

http://www.scilifelab.se/research/scientific-highlights/ruff

Inheritance: From planned matings, Lank et al. (1995) concluded that the two "morphs" of mating strategy in this species (independent and satellite) are determined by the segregation of two alleles at an autosomal locus, with satellite allele (S) being dominant to the independent allele (s). Lank et al. (2013) attributed the "faeder" morph to a dominant allele, but were not sure whether it was part of the S locus.

Molecular basis: Two independent papers published simultaneously online in 2015 and as adjacent papers in 2016 (Lamichhaney et al., 2016; Küpper et al., 2016) showed that the two variant morphs (satellites and faeders) are associated with a 4.5Mb inversion on the ruff orthologue of chicken chromosome GGA11 which, due to the well-known lethality of recombinants within an inversion, has created a supergene determining male breeding behaviour, body size and plumage colour. The large sequence divergence between the wild-type and inverted variant (1.4%) indicates that the inversion happened about 4 million years ago. The inversion disrupts an essential gene (CENPN) and is therefore lethal in the homozygous condition, which means that it has been maintained as a balanced polymorphism for millions of years. Furthermore, some 500,000 years ago, the inverted supergene recombined with the wild-type allele creating a second version. Faeders possess one copy of the original inverted supergene, satellite males have one copy of the newer recombinant version, and independents lack either version. The inverted region contains about 90 genes, which include five genes (e.g. HSD17B2) affecting the metabolism of steroid hormones and the MC1R gene that is assumed to explain the white colour in satellites. (based on text kindly provided by Leif Andersson)

Associated genes:

Symbol Description Species Chr Location OMIA gene details page Other Links
CENPN centromere protein N Philomachus pugnax - no genomic information (-..-) CENPN Homologene, Ensembl, NCBI gene
HSD17B2 hydroxysteroid (17-beta) dehydrogenase 2 Philomachus pugnax - no genomic information (-..-) HSD17B2 Homologene, Ensembl, NCBI gene
MC1R melanocortin 1 receptor (alpha melanocyte stimulating hormone receptor) Philomachus pugnax - no genomic information (-..-) MC1R Homologene, Ensembl, NCBI gene

Variants

By default, variants are sorted chronologically by year of publication, to provide a historical perspective.

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Breed(s) Variant Phenotype Gene Allele Type of Variant Reference Sequence Chr. g. or m. c. or n. p. Verbal Description EVA ID Year Published PubMed ID(s) Acknowledgements
Male body size/courtship behaviour CENPN inversion "a 4.5Mb inversion on the ruff orthologue of chicken chromosomr GGA11 which, due to the well-known lethality of recombinants within an inversion, has created a supergene determining male breeding behaviour, body size and plumage colour" 2016 26569123

References


Note: the references are listed in reverse chronological order (from the most recent year to the earliest year), and alphabetically by first author within a year.
2016 Küpper, C., Stocks, M., Risse, J.E., Dos Remedios, N., Farrell, L.L., McRae, S.B., Morgan, T.C., Karlionova, N., Pinchuk, P., Verkuil, Y.I., Kitaysky, A.S., Wingfield, J.C., Piersma, T., Zeng, K., Slate, J., Blaxter, M., Lank, D.B., Burke, T. :
A supergene determines highly divergent male reproductive morphs in the ruff. Nat Genet 48:79-83, 2016. Pubmed reference: 26569125. DOI: 10.1038/ng.3443.
Lamichhaney, S., Fan, G., Widemo, F., Gunnarsson, U., Thalmann, D.S., Hoeppner, M.P., Kerje, S., Gustafson, U., Shi, C., Zhang, H., Chen, W., Liang, X., Huang, L., Wang, J., Liang, E., Wu, Q., Lee, S.M., Xu, X., Höglund, J., Liu, X., Andersson, L. :
Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat Genet 48:84-8, 2016. Pubmed reference: 26569123. DOI: 10.1038/ng.3430.
2015 Callaway, E. :
'Supergene’ determines wading birds’ sex strategy Nature news :, 2015. DOI: 10.1038/nature.2015.18802 .
Jiggins, C.D. :
A flamboyant behavioral polymorphism is controlled by a lethal supergene. Nat Genet 48:7-8, 2015. Pubmed reference: 26711109. DOI: 10.1038/ng.3472.
2014 Farrell, L.L., Küpper, C., Burke, T., Lank, D.B. :
Major breeding plumage color differences of male ruffs (Philomachus pugnax) are not associated with coding sequence variation in the MC1R gene. J Hered 106:211-5, 2014. Pubmed reference: 25534935. DOI: 10.1093/jhered/esu079.
2013 Lank, D.B., Farrell, L.L., Burke, T., Piersma, T., McRae, S.B. :
A dominant allele controls development into female mimic male and diminutive female ruffs. Biol Lett 9:20130653, 2013. Pubmed reference: 24196515. DOI: 10.1098/rsbl.2013.0653.
2006 Jukema, J., Piersma, T. :
Permanent female mimics in a lekking shorebird. Biol Lett 2:161-4, 2006. Pubmed reference: 17148353. DOI: 10.1098/rsbl.2005.0416.
1999 Lank, D.B., Coupe, M., Wynne-Edwards, K.E. :
Testosterone-induced male traits in female ruffs (Philomachus pugnax): autosomal inheritance and gender differentiation. Proceedings of the Royal Society, Series B: Biological Sciences 266:2323–2330, 1999.
1995 Lank, D.B., Smith, C.M., Hanotte, O., Burke, T., Cooke, F. :
Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax. Nature 378:59-62, 1995.

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