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Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks

Nature volume 428, pages 717–723 (2004)Cite this article

A Corrigendum to this article was published on 23 February 2006

Abstract

Hindlimb loss has evolved repeatedly in many different animals by means of molecular mechanisms that are still unknown. To determine the number and type of genetic changes underlying pelvic reduction in natural populations, we carried out genetic crosses between threespine stickleback fish with complete or missing pelvic structures. Genome-wide linkage mapping shows that pelvic reduction is controlled by one major and four minor chromosome regions. Pitx1 maps to the major chromosome region controlling most of the variation in pelvic size. Pelvic-reduced fish show the same left–right asymmetry seen in Pitx1 knockout mice, but do not show changes in Pitx1 protein sequence. Instead, pelvic-reduced sticklebacks show site-specific regulatory changes in Pitx1 expression, with reduced or absent expression in pelvic and caudal fin precursors. Regulatory mutations in major developmental control genes may provide a mechanism for generating rapid skeletal changes in natural populations, while preserving the essential roles of these genes in other processes.

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Figure 1: Genetic architecture of pelvic reduction in a cross between marine and Paxton benthic sticklebacks.
Figure 2: Structure and sequence of the stickleback Pitx1 locus.
Figure 3: Pitx1 is expressed in the prospective pelvic region of marine but not Paxton benthic sticklebacks.
Figure 4: Site-specific regulatory changes of Pitx1 expression.
Figure 5: Comparison of pelvic reduction in laboratory and natural populations.

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Acknowledgements

We thank S. Mori for providing marine sticklebacks; E. Elfarsdóttir, G. I. Gudbrandsson, L. E. Jónsdóttir, S. Ingólfsdóttir and K. Einarsdóttir for collecting Icelandic sticklebacks and scoring the parental population from Vífilsstadavatn; and F. Chan and members of the Kingsley laboratory for discussions. This work was supported in part by grants from the National Institutes of Health (to D.M.K.), the Natural Sciences and Engineering Research Council of Canada and the Canada Foundation for Innovation (to D.S.), and the City of Gardabaer (to B.J.); a Helen Hay Whitney Foundation postdoctoral fellowship (to M.D.S.); and a Howard Hughes Medical Institute predoctoral fellowship (to M.E.M). D.S. is a Canada Research Chair, and D.M.K. is an Associate Investigator of the Howard Hughes Medical Institute.

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Author notes

  1. Michael D. Shapiro, Melissa E. Marks and Catherine L. Peichel: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Developmental Biology and HHMI, Stanford University School of Medicine, Stanford, California, 94305-5329, USA

    Michael D. Shapiro, Melissa E. Marks, Benjamin K. Blackman, Kirsten S. Nereng & David M. Kingsley

  2. Fred Hutchinson Cancer Research Center, Seattle, Washington, 98109, USA

    Catherine L. Peichel

  3. Institute of Freshwater Fisheries, Holar Agricultural College, IS-551, Saudarkrokur, Iceland

    Bjarni Jónsson

  4. Department of Zoology, University of British Columbia, 6270 University Blvd, V6T 1Z4, Vancouver, Canada

    Dolph Schluter

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Correspondence to David M. Kingsley.

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Supplementary information

Supplementary Information

List of microsatellite markers used in Figure 1 of main text; and Supplementary Table 1: Comparison of the effect of modifier QTL in animals with different genotypes at the Pitx1 locus. (DOC 100 kb)

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Shapiro, M., Marks, M., Peichel, C. et al. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717–723 (2004). https://doi.org/10.1038/nature02415

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