Antarctica as an evolutionary arena during the Cenozoic global cooling

It is striking to observe that species richness is not evenly distributed across the surface of the planet. Current species diversity indeed decreases toward the poles, with Antarctica for instance being depauperate compared to tropical regions. This ubiquitous pattern has long attracted the attention of naturalists and more recently of evolutionary biologists and paleontologists to understand why species diversity peaks at the equator. However, it remains poorly understood how polar biodiversity originated and diversified. Antarctica is currently defined as three large biogeographic regions: the Maritime Antarctic, the sub-Antarctic, and the Continental Antarctic. The Maritime Antarctic region is largely separated from the rest of the world’s oceans due to the Antarctic Circumpolar Current (ACC), differences in temperature along the Antarctic Polar Front (APF), and the presence of a deep sea surrounding the Antarctic shelf (1). The sub-Antarctic region consists of dozens of islands contained within the APF, generally characterized by the presence of tundra (absent from the Continental Antarctic) and fellfield habitats. As for the Continental Antarctic region, it is mostly uninhabitable, with less than 0.5% of its surface being ice-free. A long-standing idea is that biodiversity in Antarctica is low, and only constituted of old and poorly diversified lineages. In PNAS, a study (2)—relying on both microevolutionary and macroevolutionary approaches—challenges this idea and shows that terrestrial life can thrive there.

Diversity and Diversification in Antarctica

Our understanding of the origin and evolution of Antarctic biodiversity has greatly improved in recent years, thanks in part to studies revealing high levels of cryptic diversity, especially for marine organisms for which species diversity is often underestimated (3). Several molecular studies also show evidence for recent colonization and high in situ diversification, thus challenging the view that Antarctica is an inhospitable frozen region where groups cannot adapt, thrive, and successfully diversify (1). Interestingly, elevated speciation rates have been recovered in marine organisms through estimations of divergence times coupled with diversification analyses in several groups (Fig. 1), such as marine fishes (4, 5) or ophiuroids (6). Unexpectedly, these studies found higher diversification rates in Antarctica than in tropical regions in the last 10 My (5, 6). Despite its isolation, Antarctica has also been shown to act as an evolutionary source of marine biodiversity (7), as evidenced by the inference of multiple out-of-Antarctica biogeographic patterns during the Cenozoic (8, 9). For terrestrial (including freshwater) organisms, however, only a few groups are currently adapted to the extreme conditions of the sub-Antarctic and Continental Antarctic (1), and there had been no evidence supporting the hypothesis that sustained episodes of diversification could have occurred for them since the onset of the global cooling of Antarctica ca. 34 Ma. The study by Baird et al. (2) elegantly questions the paradigm related to the diversification of terrestrial organisms in Antarctica and reveals that the sub-Antarctic region acted as a dynamic evolutionary arena for a beetle lineage during major cooling episodes and glacial cycles, spurring a significant radiation that parallels some of the adaptive radiations experienced by marine lineages (e.g., ref. 10).

Fig. 1.

Cenozoic environmental changes and diversification patterns in Antarctica. Molecular dated phylogenies (2, 4–6, 16) provide evidence of the timing of diversification in Antarctica for marine (blue silhouettes) and terrestrial (black silhouettes) groups. One terrestrial clade (Ectemnorhini weevils; ref. 1) and one marine clade (Antarctic icefishes; ref. 4) show increasing diversification toward the present (yellow stars) potentially correlated to climate cooling. Estimates of Antarctic endemics species for each group are provided on the Right. The Cenozoic climate curve indicates the main events of global cooling (13). P, Pleistocene; Pli., Pliocene. Organism images credit (Top to Bottom): Phlyopic/Jonathan Lawley; Phylopic/Lily Hughes; Phylopic/Mathilde Cordellier, licensed under CC BY-NC 3.0; Phylopic/Steven Traver; Phlyopic/Ernst Haeckel and T. Michael Keesey; Phylopic/JCGiron, licensed under CC BY 3.0; F.C. and G.K.; Phlyopic/Kamil S. Jaron; Phylopic/Fernando Carezzano; and Phylopic/Birgit Lang, licensed under CC BY 3.0.

Shifting Biomes as Potential Evolutionary Arenas

Despite its scarcity, the Antarctic Eocene fossil record shows that terrestrial life was once rich, as exemplified by the presence of Nothofagus forests, frogs (11), and diverse birds and mammals (e.g., ref. 12). All these groups progressively went extinct in Antarctica due to the major global cooling that began at the Eocene–Oligocene boundary (13), coinciding with the opening of the Drake Passage and the associated intensification of the ACC. Drastic environmental changes led to massive ecosystem turnover, precipitating the downfall of angiosperm communities and of their associated fauna. Further major cooling events occurred during the middle and late Miocene climate transition (ca. 14 and 7 Ma, respectively), increasing the dominance of fellfield terrestrial habitats (even in the sub-Antarctic region), and leading to the disappearance of tundra habitat from continental Antarctica (14) and to the growth of ice sheets (13). Since then, it was thought the continent and surrounding islands have been depauperate of life, or only contain a few relict lineages. This seems true for most terrestrial groups such as snails (only one autochthonous species has been observed), or in most insect lineages that are only represented by one (e.g., Hemiptera, Hymenoptera) or a handful of species (e.g., Diptera, Lepidoptera).

However, this is not the case for the insect group studied by Baird et al. (2), the Ectemnorhini weevils (Coleoptera: Curculionidae). This group consists of 36 known species, all of which are distributed in the sub-Antarctic region, along the APF in the Kerguelen Province (i.e., Crozet, Kerguelen, Prince Edward Islands, and Heard Island and McDonald Islands archipelagos). All species are flightless and present several unusual life history traits, with one clade exhibiting unique algae- and moss-feeding specialization (“cryptogam feeders” Bothrometopus clade) and even including a so-called “marine” species (Palirhoeus eatoni) strikingly adapted to the supralittoral zone. Using a combination of phylogenomics (515 genes; fossil-calibrated tree of 12 Ectemnorhini species and 87 outgroups) and phylogenetics (a five-gene phylogeny of Ectemnorhini including two-thirds of known species), Baird et al. (2) inferred that this clade colonized the sub-Antarctic islands between 55 and 38 Ma (Eocene) from Africa, likely through the Crozet archipelago. Such a journey would have involved a long-distance dispersal, which may seem unfeasible for these flightless insects. However, throughout their evolutionary history, these weevils have repeatedly colonized the sub-Antarctic islands, especially in the last 10 My, despite these islands being isolated by >1,000 km of ocean in the ACC. Even more surprising is that a single species, Palirhoeus eatoni, is also distributed across several of these islands, thus testifying to the ability of these weevils to cross oceanic barriers. With knowledge on weevil resilience to dehydration and starvation, Baird et al. (2) propose the hypothesis that bird-mediated dispersal can explain the biogeographic pattern and the numerous intraisland dispersal events. Indeed, Antarctic seabirds regularly fly hundreds of kilometers in a single day when migrating between sub-Antarctic islands, and it is likely that invertebrates can attach to their feathers and then disperse with their carrier.

Baird et al. found evidence that the weevil clade is diversifying faster today than at its origin (especially in the last 5 My), which goes against the general trend of diversification slowdown after origination.

Importantly, Baird et al. (2) found evidence that the weevil clade is diversifying faster today than at its origin (especially in the last 5 My), which goes against the general trend of diversification slowdown after origination (15). Consistent with the inferred increase in speciation rates, additional phylogeographic analyses focusing on Palirhoeus eatoni (population structure analysis based on 5,859 single-nucleotide polymorphisms) also indicated that this lineage is in the process of incipient speciation, supporting the hypothesis that the clade is currently expanding. Using multiple diversification approaches, Baird et al. (2) inferred that speciation rates correlate with trends in global cooling, such that weevils diversified faster when climate cooled and when fellfield habitats became dominant. They postulate that changes in Antarctic conditions likely promoted their diversification on novel polar niches, in relation for instance with adaptation to cryptogams and better freezing tolerance in association with flightlessness. This diversification pattern parallels the specific adaptations observed in Antarctic fishes (4, 10) and penguins (16), which also led to successful recent radiations.

Implications

The study by Baird et al. (2) calls for reevaluation of the paradigm on the origin and evolution of species diversity in Antarctica during the Cenozoic. This study demonstrates that diversification of Antarctic terrestrial organisms may mirror those of marine organisms. This unveiling calls for more studies in other terrestrial groups, especially for those that potentially house high levels of cryptic biodiversity such as springtails (17) or tardigrades (18). This study on weevils should encourage further studies to infer dated phylogenies for Antarctic groups, as it is of paramount importance to determine their mode and tempo of diversification and assess whether there are similar trends in relation with known paleoenvironmental changes (Fig. 1). Studying these Antarctic groups can also bring light to the evolution of the latitudinal diversity gradient, in particular to understand why some regions are species-poor compared to others but show high in situ diversification.

Even if Antarctica and the surrounding islands are isolated and inhospitable for humans, they are not spared from human-driven threats and their regional biodiversity remains poorly protected (19). If most groups follow a similar diversification pattern to Ectemnorhini weevils in relation to climate cooling, they may be highly vulnerable to global warming. The Antarctic ice cap is indeed melting at unprecedented rates (20), which may destabilize the ecosystem relied upon by this regional pool of species that may currently be in the process of diversifying.