Inferred genetic architecture underlying evolution in a fossil stickleback lineage

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.

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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.

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).

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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.

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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.

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Correspondence to Yoel E. Stuart.

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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.

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

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