Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Inferred genetic architecture underlying evolution in a fossil stickleback lineage

Nature Ecology & Evolution volume 4, pages 1549–1557 (2020)Cite this article

Subjects

Abstract

Inferring the genetic architecture of evolution in the fossil record is difficult because genetic crosses are impossible, the acquisition of DNA is usually impossible and phenotype–genotype maps are rarely obvious. However, such inference is valuable because it reveals the genetic basis of microevolutionary change across many more generations than is possible in studies of extant taxa, thereby integrating microevolutionary process and macroevolutionary pattern. Here, we infer the genetic basis of pelvic skeleton reduction in Gasterosteus doryssus, a Miocene stickleback fish from a finely resolved stratigraphic sequence that spans nearly 17,000 years. Reduction in pelvic score, a categorical measure of pelvic structure, resulted primarily from reciprocal frequency changes of two discrete phenotypic classes. Pelvic vestiges also showed left-side larger asymmetry. These patterns implicate Pitx1, a large-effect gene whose deletion generates left-side larger asymmetry of pelvic vestiges in extant, closely related Gasterosteus aculeatus. In contrast, reductions in the length of the pelvic girdle and pelvic spines resulted from directional shifts of unimodal, continuous trait distributions, suggesting an additional suite of genes with minor, additive pelvic effects, again like G. aculeatus. Similar genetic architectures explain shared but phyletically independent patterns across 10 million years of stickleback evolution.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The pelvic vestige was larger on the left side in significantly more than half of all specimens of G. doryssus with vestigial pelvic structures.
Fig. 2: Mean PS declines through time in temporal sequence L after a delay.
Fig. 3: Relative frequency distributions of PS through time from temporal sequence K.
Fig. 4: Reduction of size-adjusted pelvic girdle and pelvic spine length in temporal sequence K began immediately after replacement of lineage I by lineage II.
Fig. 5: Frequency distributions of pelvic girdle and pelvic spine length for specimens from temporal sequence K.

Similar content being viewed by others

Data availability

Data are available at Dryad (https://doi.org/10.5061/dryad.02v6wwq18).

Code availability

Code is available at Dryad (https://doi.org/10.5061/dryad.02v6wwq18).

References

  1. Bell, M. A., Baumgartner, J. V. & Olson, E. C. Patterns of temporal change in single morphological characters of a Miocene stickleback fish. Paleobiology 11, 258–271 (1985).

    Article  Google Scholar 

  2. Bell, M. A. Implications of a fossil stickleback assemblage for Darwinian gradualism. J. Fish. Biol. 75, 1977–1999 (2009).

    Article  CAS  PubMed  Google Scholar 

  3. Bell, M. A., Travis, M. P. & Blouw, D. M. Inferring natural selection in a fossil threespine stickleback. Paleobiology 32, 562–577 (2006).

    Article  Google Scholar 

  4. Hunt, G., Bell, M. A. & Travis, M. P. Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evolution 62, 700–710 (2008).

    Article  PubMed  Google Scholar 

  5. Klepaker, T., Østbye, K. & Bell, M. A. Regressive evolution of the pelvic complex in stickleback fishes: a study of convergent evolution. Evol. Ecol. Res. 15, 413–435 (2013).

    Google Scholar 

  6. Bell, M. A., Ortí, G., Walker, J. A. & Koenings, J. P. Evolution of pelvic reduction in threespine stickleback fish: a test of competing hypotheses. Evolution 47, 906–914 (1993).

    Article  PubMed  Google Scholar 

  7. Chan, Y. F. et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302–305 (2010).

    Article  CAS  PubMed  Google Scholar 

  8. Cole, N. J., Tanaka, M., Prescott, A. & Tickle, C. Expression of limb initiation genes and clues to the morphological diversification of threespine stickleback. Curr. Biol. 13, R951–R952 (2003).

    Article  CAS  PubMed  Google Scholar 

  9. Shapiro, M. D. et al. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717–723 (2004).

    Article  CAS  PubMed  Google Scholar 

  10. Cresko, W. A. et al. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc. Natl Acad. Sci. USA 101, 6050–6055 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Coyle, S. M., Huntingford, F. A. & Peichel, C. L. Parallel evolution of Pitx1 underlies pelvic reduction in Scottish threespine stickleback (Gasterosteus aculeatus). J. Hered. 98, 581–586 (2007).

    Article  CAS  PubMed  Google Scholar 

  12. Xie, K. T. et al. DNA fragility in the parallel evolution of pelvic reduction in stickleback fish. Science 363, 81–84 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bell, M. A., Khalef, V. & Travis, M. P. Directional asymmetry of pelvic vestiges in threespine stickleback. J. Exp. Zool. B Mol. Dev. Evol. 308B, 189–199 (2007).

    Article  Google Scholar 

  14. Palmer, A. R. Symmetry breaking and the evolution of development. Science 306, 828–833 (2004).

    Article  CAS  PubMed  Google Scholar 

  15. Marcil, A., Dumontier, É., Chamberland, M., Camper, S. A. & Drouin, J. Pitx1 and Pitx2 are required for development of hindlimb buds. Development 130, 45–55 (2003).

    Article  CAS  PubMed  Google Scholar 

  16. Shapiro, M. D., Bell, M. A. & Kingsley, D. M. Parallel genetic origins of pelvic reduction in vertebrates. Proc. Natl Acad. Sci. USA 103, 13753–13758 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bell, M. A. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 438–471 (Oxford Univ. Press, 1994).

  18. Peichel, C. L. et al. The genetic architecture of divergence between threespine stickleback species. Nature 414, 901–905 (2001).

    Article  CAS  PubMed  Google Scholar 

  19. Rollins, J. L., Lohman, B. K. & Bell, M. A. Does ion limitation select for pelvic reduction in threespine stickleback (Gasterosteus aculeatus)? Evol. Ecol. Res. 16, 101–120 (2014).

    Google Scholar 

  20. Reimchen, T. E. Spine deficiency and polymorphism in a population of Gasterosteus aculeatus: an adaptation to predators? Can. J. Zool. 58, 1232–1244 (1980).

    Article  Google Scholar 

  21. Reimchen, T. E. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 240–276 (Oxford Univ. Press, 1994).

  22. Hoogland, R., Morris, D. & Tinbergen, N. The spines of sticklebacks (Gasterosteus and Pygosteus) as a means of defense against predators (Perca and Esox). Behaviour 10, 205–236 (1956).

    Article  Google Scholar 

  23. Baumgartner, J. V. A new fossil ictalurid catfish from the Miocene middle member of the Truckee Formation, Nevada. Copeia 1982, 38–46 (1982).

    Article  Google Scholar 

  24. Stearley, R. F. & Smith, G. R. Fishes of the Mio-Pliocene western snake river plain and vicinity. Misc. Publ. Mus. Zool. Univ. Mich. 204, 1–43 (2016).

    Google Scholar 

  25. Baker, J. A. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 144–187 (Oxford Univ. Press, 1994).

  26. Bell, M. A. Interacting evolutionary constraints in pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces, Gasterosteidae). Biol. J. Linn. Soc. Lond. 31, 347–382 (1987).

    Article  Google Scholar 

  27. Bell, M. A. & Harris, E. I. Developmental osteology of the pelvic complex of Gasterosteus aculeatus. Copeia 1985, 789–792 (1985).

    Article  Google Scholar 

  28. Schmid, L. & Sánchez-Villagra, M. R. Potential genetic bases of morphological evolution in the Triassic fish Saurichthys. J. Exp. Zool. B Mol. Dev. Evol. 314B, 519–526 (2010).

    Article  Google Scholar 

  29. Meredith, R. W., Gatesy, J., Murphy, W. J., Ryder, O. A. & Springer, M. S. Molecular decay of the tooth gene Enamelin (ENAM) mirrors the loss of enamel in the fossil record of placental mammals. PLoS Genet. 5, e1000634 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Qu, Q., Haitina, T., Zhu, M. & Ahlberg, P. E. New genomic and fossil data illuminate the origin of enamel. Nature 526, 108–111 (2015).

    Article  CAS  PubMed  Google Scholar 

  31. Zhu, M. et al. A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502, 188–193 (2013).

    Article  CAS  PubMed  Google Scholar 

  32. Zhu, M. Bone gain and loss: insights from genomes and fossils. Natl Sci. Rev. 1, 490–492 (2014).

    Article  CAS  Google Scholar 

  33. Hunt, G. Evolutionary divergence in directions of high phenotypic variance in the ostracode genus Poseidonamicus. Evolution 61, 1560–1576 (2007).

    Article  PubMed  Google Scholar 

  34. Thompson, J. R. et al. Reorganization of sea urchin gene regulatory networks at least 268 million years ago as revealed by oldest fossil cidaroid echinoid. Sci. Rep. 5, 15541 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Organ, C. L., Janes, D. E., Meade, A. & Pagel, M. Genotypic sex determination enabled adaptive radiations of extinct marine reptiles. Nature 461, 389–392 (2009).

    Article  CAS  PubMed  Google Scholar 

  36. Organ, C. L., Shedlock, A. M., Meade, A., Pagel, M. & Edwards, S. V. Origin of avian genome size and structure in non-avian dinosaurs. Nature 446, 180–184 (2007).

    Article  CAS  PubMed  Google Scholar 

  37. Organ, C. L. & Shedlock, A. M. Palaeogenomics of pterosaurs and the evolution of small genome size in flying vertebrates. Biol. Lett. 5, 47–50 (2009).

    Article  PubMed  Google Scholar 

  38. Conte, G. L., Arnegard, M. E., Peichel, C. L. & Schluter, D. The probability of genetic parallelism and convergence in natural populations. Proc. Biol. Sci. 279, 5039–5047 (2012).

    PubMed  PubMed Central  Google Scholar 

  39. Rennison, D. J., Stuart, Y. E., Bolnick, D. I. & Peichel, C. L. Ecological factors and morphological traits are associated with repeated genomic differentiation between lake and stream stickleback. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 374, 20180241 (2019).

    Article  CAS  Google Scholar 

  40. Szeto, D. P. et al. Role of the Bicoid-related homeodomain factor Pitx1 in specifying hindlimb morphogenesis and pituitary development. Genes Dev. 13, 484–494 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Thompson, A. C. et al. A novel enhancer near the Pitx1 gene influences development and evolution of pelvic appendages in vertebrates. eLife 7, e38555 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Bell, M. A., Stewart, J. D. & Park, P. J. The world’s oldest fossil threespine stickleback fish. Copeia 2009, 256–265 (2009).

    Article  Google Scholar 

  43. Rawlinson, S. E. & Bell, M. A. A stickleback fish (Pungitius) from the Neogene Sterling Formation, Kenai Peninsula, Alaska. J. Paleontol. 56, 583–588 (1982).

    Google Scholar 

  44. Rohlf, F. J. tpsDIG v.2.10 (2006).

  45. Bowne, P. S. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 28–60 (Oxford Univ. Press, 1994).

  46. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).

  47. Lleonart, J., Salat, J. & Torres, G. J. Removing allometric effects of body size in morphological analysis. J. Theor. Biol. 205, 85–93 (2000).

    Article  CAS  PubMed  Google Scholar 

  48. Oke, K. B. et al. Does plasticity enhance or dampen phenotypic parallelism? A test with three lake-stream stickleback pairs. J. Evol. Biol. 29, 126–143 (2016).

    Article  CAS  PubMed  Google Scholar 

  49. Stuart, Y. E. et al. Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nat. Ecol. Evol. 1, 0158 (2017).

    Article  Google Scholar 

  50. Hartigan, J. A. & Hartigan, P. M. The dip test of unimodality. Ann. Stat. 13, 70–84 (1985).

    Article  Google Scholar 

  51. Maechler, M. diptest: Hartigan’s dip statistic for unimodality—corrected v.0.75-7 (2016); https://rdrr.io/cran/diptest/

Download references

Acknowledgements

Cyprus Industrial Minerals, CR Minerals and T. Sumner of World Minerals allowed us to collect fossils on their property. We thank the people acknowledged in ref. 3 plus D. Arcieri, K. Brudvik, N. J. Buck, F. Castelli, R. Obeng, J. Qiao, C. Redman and T. T. Zhang for field and laboratory assistance; F. J. Rohlf for statistical advice; M. D. Houseman for sharing his extensive knowledge of Truckee Formation palaeoecology and taphonomy. C. W. Chan measured all pelvic vestiges for the asymmetry analysis. We thank J. Jernvall, D. M. Kingsley, S. Chenoweth, R. Bonduriansky, Y. F. Chan, J. Weber, A. Kamath, R. Duckworth and S. Swank for helpful comments and discussion. This research was supported by National Science Foundation (NSF) grant nos. BSR-8111013, EAR-9870337 and DEB-0322818, the Center for Field Research (Earthwatch), the National Geographic Society (no. 2869–84), National Institutes of Health grant no. R01 GM124330-01 to M.A.B. and NSF grant nos. DEB-1456462 and DEB-2003457 to Y.E.S.

Author information

Authors and Affiliations

  1. Department of Biology, Loyola University Chicago, Chicago, IL, USA

    Yoel E. Stuart

  2. Department of Biological Sciences, Rowan University, Glassboro, NJ, USA

    Matthew P. Travis

  3. University of California Museum of Paleontology, Berkeley, CA, USA

    Michael A. Bell

Authors
  1. Yoel E. Stuart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew P. Travis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael A. Bell
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.A.B., M.P.T. and Y.E.S. designed the research. M.A.B. supervised sample and data collection. M.A.B. and M.P.T. collected the data. Y.E.S. analysed the data, created the figures and wrote the paper. M.A.B., M.P.T. and Y.E.S. jointly edited the paper.

Corresponding author

Correspondence to Yoel E. Stuart.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Gasterosteus doryssus fossils.

High-armored (top) and low-armored (middle) specimens of Gasterosteus doryssus. Dorsal spines 1, 2, and 3 (D1- D3) are noted, as are pelvic spine and pelvic girdle lengths. Standard length is measured from the anterior tip of the premaxilla to the posterior end of the hypural plate. Images of pelvic girdles (bottom) showing the range of pelvic phenotypes and their pelvic scores (PS). (Extended Data Fig. 3 shows the full distribution of PS phenotypes.) Contrast has been digitally enhanced to emphasize phenotypic differences.

Extended Data Fig. 2 Stratigraphic correlation in years for temporal sequences D (Bell et al. 1985), L (Bell et al. 2006) and K (this study).

L and K are used in this study. They comprise separate specimens but came from the same stratigraphic section in the same exposure.

Extended Data Fig. 3 Examples of pelvic scores (PS).

Drawings are from Bell (1987) and photographs are specimens from temporal sequence K. Anterior is to the left, except for the drawing of PS 3.0. Abbreviations are AB, ascending branch; AP, anterior process; PFR, pelvic fin ray; PP, posterior process; PS, pelvic spine; S, median suture between left and right pelvic girdles. PP for any score may be separate bilateral elements or fused. No drawing was made for PS 1.4, and there is no photograph of PS 2.8 because none was present in the photographed K specimens.

Supplementary information

Supplementary Information

Size correction protocol, Supplementary Tables 1–5.

Reporting Summary

Peer Review Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stuart, Y.E., Travis, M.P. & Bell, M.A. Inferred genetic architecture underlying evolution in a fossil stickleback lineage. Nat Ecol Evol 4, 1549–1557 (2020). https://doi.org/10.1038/s41559-020-01287-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-020-01287-x

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing