Historical contingency shapes adaptive radiation in Antarctic fishes

Abstract

Adaptive radiation illustrates links between ecological opportunity, natural selection and the generation of biodiversity. Central to adaptive radiation is the association between a diversifying lineage and the evolution of phenotypic variation that facilitates the use of new environments or resources. However, is not clear whether adaptive evolution or historical contingency is more important for the origin of key phenotypic traits in adaptive radiation. Here we use targeted sequencing of >250,000 loci across 46 species to examine hypotheses concerning the origin and diversification of key traits in the adaptive radiation of Antarctic notothenioid fishes. Contrary to expectations of adaptive evolution, we show that notothenioids experienced a punctuated burst of genomic diversification and evolved key skeletal modifications before the onset of polar conditions in the Southern Ocean. We show that diversifying selection in pathways associated with human skeletal dysplasias facilitates ecologically important variation in buoyancy among Antarctic notothenioid species, and demonstrate the sufficiency of altered trip11, col1a2 and col1a1a function in zebrafish (Danio rerio) to phenocopy skeletal reduction in Antarctic notothenioids. Rather than adaptation being driven by the cooling of the Antarctic, our results highlight the role of historical contingency in shaping the adaptive radiation of notothenioids. Understanding the historical and environmental context for the origin of key traits in adaptive radiations extends beyond reconstructing events that result in evolutionary innovation, as it also provides a context in forecasting the effects of climate change on the stability and evolvability of natural populations.

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Fig. 1: Punctuated elevation in genomic diversification before ecological change and adaptive radiation.
Fig. 2: Skeletal reduction occurs before the cryonotothenioid radiation.
Fig. 3: Skeletal genes under diversifying selection uncover genetic mechanisms regulating bone density.

Data availability

The sequencing data have been deposited in the NCBI database as Bioproject PRJNA531677. Assembled contig data have been deposited in the Zenodo repository (10.5281/zenodo.2628936).

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Acknowledgements

The authors thank E. Snay and L. Oberg in the Department of Nuclear Medicine and Molecular Imaging at Boston Children’s Hosptial for assistance in computed tomography of adult specimens. This work was supported in part by American Heart Association Postdoctoral Fellowship (No. 17POST33660801) to J.M.D., the John Simon Guggenheim Fellowship and William F. Milton Fund awarded to M.P.H., the National Science Foundation (NSF) grant (No. PLR-1444167 to H.W.D.), the NSF grant (No. IOS-1755242 to A.D.), the Bingham Oceanographic Fund from the Peabody Museum of Natural History, and Yale University, as well as the Children’s Orthopaedic Surgery Foundation at Boston Children’s Hospital. This is contribution No. 389 from the Marine Science Center at Northeastern University.

Author information

J.M.D., H.W.D. and M.P.H. conceived and designed the study. J.M.D., P.S. and M.B.H. performed the experiments. J.M.D., A.D., T.J.N., D.J.M., H.W.D. and M.P.H. analysed the data. J.M.D., A.D. and T.J.N. wrote the first drafts of the manuscript. All authors contributed to the writing of the final manuscript.

Correspondence to Jacob M. Daane or H. William Detrich III or Matthew P. Harris.

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Daane, J.M., Dornburg, A., Smits, P. et al. Historical contingency shapes adaptive radiation in Antarctic fishes. Nat Ecol Evol 3, 1102–1109 (2019). https://doi.org/10.1038/s41559-019-0914-2

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