The Southern Ocean around Antarctica is among the most rapidly warming regions on Earth, but has experienced episodic climate change during the past 40 million years. It remains unclear how ancient periods of climate change have shaped Antarctic biodiversity. The origin of antifreeze glycoproteins (AFGPs) in Antarctic notothenioid fishes has become a classic example of how the evolution of a key innovation in response to climate change can drive adaptive radiation. By using a time-calibrated molecular phylogeny of notothenioids and reconstructed paleoclimate, we demonstrate that the origin of AFGP occurred between 42 and 22 Ma, which includes a period of global cooling approximately 35 Ma. However, the most species-rich lineages diversified and evolved significant ecological differences at least 10 million years after the origin of AFGPs, during a second cooling event in the Late Miocene (11.6–5.3 Ma). This pattern indicates that AFGP was not the sole trigger of the notothenioid adaptive radiation. Instead, the bulk of the species richness and ecological diversity originated during the Late Miocene and into the Early Pliocene, a time coincident with the origin of polar conditions and increased ice activity in the Southern Ocean. Our results challenge the current understanding of the evolution of Antarctic notothenioids suggesting that the ecological opportunity that underlies this adaptive radiation is not linked to a single trait, but rather to a combination of freeze avoidance offered by AFGPs and subsequent exploitation of new habitats and open niches created by increased glacial and ice sheet activity.

Investigations in recent years of the ecological structure and processes of the Southern Ocean have almost exclusively taken a bottom-up, forcing-by-physical-processes approach relating various species' population trends to climate change. Just 20 years ago, however, researchers focused on a broader set of hypotheses, in part formed around a paradigm positing interspecific interactions as central to structuring the ecosystem (forcing by biotic processes, top-down), and particularly on a “krill surplus” caused by the removal from the system of more than a million baleen whales. Since then, this latter idea has disappeared from favour with little debate. Moreover, it recently has been shown that concurrent with whaling there was a massive depletion of finfish in the Southern Ocean, a finding also ignored in deference to climate-related explanations of ecosystem change. We present two examples from the literature, one involving gelatinous organisms and the other involving penguins, in which climate has been used to explain species' population trends but which could better be explained by including species interactions in the modelling. We conclude by questioning the almost complete shift in paradigms that has occurred and discuss whether it is leading Southern Ocean marine ecological science in an instructive direction.