Fifty million years of beetle evolution along the Antarctic Polar Front

Abstract

Global cooling and glacial–interglacial cycles since Antarctica’s isolation have been responsible for the diversification of the region’s marine fauna. By contrast, these same Earth system processes are thought to have played little role terrestrially, other than driving widespread extinctions. Here, we show that on islands along the Antarctic Polar Front, paleoclimatic processes have been key to diversification of one of the world’s most geographically isolated and unique groups of herbivorous beetles—Ectemnorhinini weevils. Combining phylogenomic, phylogenetic, and phylogeographic approaches, we demonstrate that these weevils colonized the sub-Antarctic islands from Africa at least 50 Ma ago and repeatedly dispersed among them. As the climate cooled from the mid-Miocene, diversification of the beetles accelerated, resulting in two species-rich clades. One of these clades specialized to feed on cryptogams, typical of the polar habitats that came to prevail under Miocene conditions yet remarkable as a food source for any beetle. This clade’s most unusual representative is a marine weevil currently undergoing further speciation. The other clade retained the more common weevil habit of feeding on angiosperms, which likely survived glaciation in isolated refugia. Diversification of Ectemnorhinini weevils occurred in synchrony with many other Antarctic radiations, including penguins and notothenioid fishes, and coincided with major environmental changes. Our results thus indicate that geo-climatically driven diversification has progressed similarly for Antarctic marine and terrestrial organisms since the Miocene, potentially constituting a general biodiversity paradigm that should be sought broadly for the region’s taxa.

Antarctica as an evolutionary arena during the Cenozoic global cooling

“…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 longdistance dispersal, which may seem unfeasible for these flightless insects.…”

“…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.…”

“…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.…”

“…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.…”