Fifty million years of beetle evolution along the Antarctic Polar Front Helena P. Bairda,1, Seunggwan Shinb,c,d, Rolf G. Oberprielere, Maurice Hulléf, Philippe Vernong, Katherine L. Moona, Richard H. Adamsh, Duane D. McKennab,c,2, and Steven L. Chowni,2 aSchool of Biological Sciences, Monash University, Clayton, VIC 3800, Australia; bDepartment of Biological Sciences, University of Memphis, Memphis, TN 38152; cCenter for Biodiversity Research, University of Memphis, Memphis, TN 38152; dSchool of Biological Sciences, Seoul National University, Seoul 08826, Republic of Korea; eAustralian National Insect Collection, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT 2601, Australia; fInstitut de Génétique, Environnement et Protection des Plantes, Institut national de recherche pour l’agriculture, l’alimentation et l’environnement, Université de Rennes, 35653 Le Rheu, France; gUniversité de Rennes, CNRS, UMR 6553 ECOBIO, Station Biologique, 35380 Paimpont, France; hDepartment of Computer and Electrical Engineering and Computer Science, Florida Atlantic University, Boca Raton, FL 33431; and iSecuring Antarctica’s Environmental Future, School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved May 6, 2021 (received for review August 24, 2020) Global cooling and glacial–interglacial cycles since Antarctica’s iso- The hypothesis that diversification has proceeded similarly in lation have been responsible for the diversification of the region’s Antarctic marine and terrestrial groups has not been tested. While marine fauna. By contrast, these same Earth system processes are the extinction of a diverse continental Antarctic biota is well thought to have played little role terrestrially, other than driving established (13), mounting evidence of significant and biogeo- widespread extinctions. Here, we show that on islands along the graphically structured Antarctic terrestrial diversity (8, 14, 15) with Antarctic Polar Front, paleoclimatic processes have been key to a long evolutionary history (6, 16) suggests the possibility of broadly diversification of one of the world’s most geographically isolated similar diversification processes across marine and terrestrial Ant- and unique groups of herbivorous beetles—Ectemnorhinini wee- arctic systems. If valid for some taxa, further tests should then be vils. Combining phylogenomic, phylogenetic, and phylogeographic sought across a wider variety of organisms. Here, we therefore approaches, we demonstrate that these weevils colonized the sub- evaluate the terrestrial applicability of the paradigm emerging for Antarctic islands from Africa at least 50 Ma ago and repeatedly Antarctic marine biodiversity—that a major cooling phase from the dispersed among them. As the climate cooled from the mid-Miocene, mid-Miocene climatic transition (14 Ma) onwards, and subsequent EVOLUTION diversification of the beetles accelerated, resulting in two species- habitat restructuring, have led to significant and ongoing diversifi- rich clades. One of these clades specialized to feed on cryptogams, cation for many taxa, including those with much older origins in the typical of the polar habitats that came to prevail under Miocene region (2, 4, 17). We do so by using one of the most well-known conditions yet remarkable as a food source for any beetle. This ’ and speciose groups from the sub-Antarctic, the herbivorous clade s most unusual representative is a marine weevil currently un- – dergoing further speciation. The other clade retained the more com- Ectemnorhinini weevils (Coleoptera: Curculionidae) (18 20). mon weevil habit of feeding on angiosperms, which likely survived Preliminary molecular studies indicate that the Ectemnorhinini, glaciation in isolated refugia. Diversification of Ectemnorhinini wee- along with numerous other terrestrial taxa, have long histories in vils occurred in synchrony with many other Antarctic radiations, in- cluding penguins and notothenioid fishes, and coincided with major Significance environmental changes. Our results thus indicate that geo- climatically driven diversification has progressed similarly for Antarc- The Antarctic environment is famously inhospitable to most tic marine and terrestrial organisms since the Miocene, potentially terrestrial biodiversity, traditionally viewed as a driver of species constituting a general biodiversity paradigm that should be sought extinction. Combining population- and species-level molecular broadly for the region’s taxa. data, we show that beetles on islands along the Antarctic Polar Front diversified in response to major climatic events over the Antarctica | species radiation | paleoclimate | herbivory | island last 50 Ma in surprising synchrony with the region’s marine or- biogeography ganisms. Unique algae- and moss-feeding habits enabled beetles to capitalize on cooling conditions, which resulted in a decline in ntarctica’s isolation, cooling, and glacial–interglacial cycles flowering plants—the typical hosts for beetles elsewhere. Ant- Aover the Cenozoic have resulted in the remarkable diversi- arctica’s cooling paleoclimate thus fostered the diversification of fication of a unique marine fauna (1, 2). The investigation of marine both terrestrial and marine life. Climatically driven evolutionary ’ radiations in Antarctica has reshaped modern understanding of processes since the Miocene may underpin much of the region s biodiversity processes, for example, by revealing a surprising inverse diversity, are still ongoing, and should be further investigated latitudinal gradient in diversification rates for fish and brittle stars among Antarctic biota. (3–5). In contrast, Antarctica’s paleoclimatic legacy for terrestrial Author contributions: H.P.B., D.D.M., and S.L.C. designed research; H.P.B., S.S., R.G.O., communities has long been considered one of widespread extinction K.L.M., D.D.M., and S.L.C. performed research; H.P.B., S.S., R.G.O., M.H., P.V., and R.H.A. due to glaciation. Evidence of terrestrial species surviving in Ant- contributed new reagents/analytic tools; H.P.B., S.S., K.L.M., and R.H.A. analyzed data; arctic glacial refugia (6) and discoveries of substantial endemic di- and H.P.B., D.D.M., and S.L.C. wrote the paper. versity and biogeographic structuring in some groups (7, 8) is The authors declare no competing interest. changing this narrative, indicating extended evolutionary histories This article is a PNAS Direct Submission. on land. Yet, such evolutionary histories remain obscured by a lack This open access article is distributed under Creative Commons Attribution License 4.0 of large-scale molecular phylogenetic work, with most Antarctic (CC BY). terrestrial research focused on small subsets of species or pop- See online for related content such as Commentaries. ulations (9, 10). The few studies that have taken a multilocus phy- 1To whom correspondence may be addressed. Email: [email protected]. logenetic approach have uncovered hidden terrestrial diversity and 2D.D.M. and S.L.C. contributed equally to this work. signals of long-term allopatric divergence (e.g., refs. 11 and 12), This article contains supporting information online at https://www.pnas.org/lookup/suppl/ hinting that Cenozoic climatic processes may have driven terrestrial doi:10.1073/pnas.2017384118/-/DCSupplemental. diversification in ways similar to that for marine life. Published June 9, 2021. PNAS 2021 Vol. 118 No. 24 e2017384118 https://doi.org/10.1073/pnas.2017384118 | 1of10 Downloaded by guest on September 24, 2021 the sub-Antarctic, extending to the Miocene or earlier [e.g., bee- with the aforementioned African genera (SI Appendix,TextS1and tles (21), midges (22), and springtails (11)]. This enables a com- Figs. S2 and S3). Tribes previously proposed to be the nearest living parison of their evolution throughout the same periods of relatives of Ectemnorhinini based on morphology, such as the environmental change that drove the diversification of Antarctic Phyllobiini (30) and the Leptopiini (18), represented in our analysis marine taxa. Moreover, the sub-Antarctic islands overlap spatially by Phyllobius and Leptopius, were not found to be close relatives with the Southern Ocean, with climates that reflect oceanic con- (Fig. 1 and SI Appendix,Figs.S2andS3). However, in agreement ditions both past and present (23, 24). While in some respects with morphological hypotheses, Christensenia from the Crozet ar- quite different to the continental Antarctic, the islands are in other chipelago was recovered as the most basal genus of the Ectemno- ways quite similar, providing a window into diversification pro- rhinini (18), estimated to have diverged from the rest of the tribe in cesses that might be sought for continental groups, especially given the Eocene (95% HPD: 37 to 57 Ma; SI Appendix,Fig.S1), fol- their age and biogeographic structuring. Both regions share many lowed by the monospecific genera Canonopsis and Disker. The two higher taxa (e.g., ref. 25), a dynamic geo-climatic history (6, 26), a most diverse clades of Ectemnorhinini, the Ectemnorhinus and the profound degree of isolation, and indications that climatic events Palirhoeus–Bothrometopus groups, diverged in the Miocene (Fig. 1). likely structured their biota (6, 8, 27). The terrestrial habitat on the continent and its surrounding islands is fragmented by large ex- Phylogenetics. A broader taxon sample of 24 Ectemnorhinini panses of ice or ocean, respectively,