Climate change, antifreeze, and the evolutionary diversification of Antarctic fishes

NEAR, THOMAS; DORNBURG, ALEX; KUHN, K; EASTMAN, J; PENNINGTON, J; PATARNELLO, T; ZANE, L; DANIEL ALFREDO FERNANDEZ; JONES, C

Proceedings of the National Academy of Sciences of the United States

National Academy of Sciences of the United States

Año: 2012 vol. 109 p. 3434 - 3439

1091-6490

The Southern Ocean around Antarctica is among the most rapidlywarming regions on Earth, but has experienced episodic climatechange during the past 40 million years. It remains unclear howancient periods of climate change have shaped Antarctic bio-diversity. The origin of antifreeze glycoproteins (AFGPs) in Ant-arctic notothenioid fishes has become a classic example of how theevolution of a key innovation in response to climate change candrive adaptive radiation. By using a time-calibrated molecularphylogeny of notothenioids and reconstructed paleoclimate, wedemonstrate that the origin of AFGP occurred between 42 and22 Ma, which includes a period of global cooling approximately35 Ma. However, the most species-rich lineages diversi fied andevolved significant ecological differences at least 10 million yearsafter the origin of AFGPs, during a second cooling event in the LateMiocene (11.6–5.3 Ma). This pattern indicates that AFGP was notthe sole trigger of the notothenioid adaptive radiation. Instead,the bulk of the species richness and ecological diversity originatedduring the Late Miocene and into the Early Pliocene, a time co-incident with the origin of polar conditions and increased ice ac-tivity in the Southern Ocean. Our results challenge the currentunderstanding of the evolution of Antarctic notothenioids sug-gesting that the ecological opportunity that underlies this adap-tive radiation is not linked to a single trait, but rather to acombination of freeze avoidance offered by AFGPs and subse-quent exploitation of new habitats and open niches created byincreased glacial and ice sheet activity.