Historical contingency shapes adaptive radiation in Antarctic fishes

• Published in: Nature ecology & evolution Vol. 3; no. 7; pp. 1102 - 1109
• Main Authors: Daane, Jacob M., Dornburg, Alex, Smits, Patrick, MacGuigan, Daniel J., Brent Hawkins, M., Near, Thomas J., William Detrich III, H., Harris, Matthew P.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01-07-2019; Nature Publishing Group
• Subjects: 45/22; 45/23; 59/78; 631/181/2474; 631/181/2806; 631/181/757; 631/601/2722; 64/116; Adaptation, Physiological; Adaptive radiation; Animals; Antarctic Regions; Biodiversity; Biological and Physical Anthropology; Biomedical and Life Sciences; Climate change; Climate effects; Comparative analysis; Contingency; Danio rerio; Ecology; Evolution; Evolution & development; Evolutionary Biology; Fishes; Humans; Life Sciences; Natural populations; Natural selection; Paleontology; Phenotypic variations; Phylogeny; Stability analysis; Zebrafish; Zoology; Antarctic Regions; Southern Ocean
• ISSN: 2397-334X; 2397-334X
• DOI: 10.1038/s41559-019-0914-2

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.
Phylogenetic comparative analysis of Antarctic notothenioid fishes reveals a burst of genomic diversification and evolution of key skeletal modifications before the onset of polar conditions in the Southern Ocean.