Survivors and colonizers: Contrasting biogeographic histories reconciled in the Antarctic freshwater copepod Boeckella poppei

Abstract

Two main hypotheses have been proposed to explain the contemporary distribution of Antarctic terrestrial biota. We assess whether the current distribution of maritime Antarctic populations of the freshwater copepod Boeckella poppei is the result of (1) a post-Last Glacial Maximum (LGM) colonization, or whether (2) the species survived in regional glacial refugia throughout the LGM and earlier glaciations. Using 438 specimens from 34 different sampling sites across Southern South America, South Georgia, South Orkney Islands, South Shetland Islands, and the Antarctic Peninsula, we analyzed mitochondrial and nuclear sequences to uncover patterns of genetic diversity and population structure. We also performed median-joining haplotype network, phylogenetic reconstruction, and divergence time analyses. Finally, we evaluated past demographic changes and historical scenarios using the Approximate Bayesian Computation (ABC) method. Our data support the existence of two clades with different and contrasting biogeographic histories. The first clade has been present in maritime Antarctica since at least the mid-Pleistocene, with the South Orkney Islands the most likely refugial area. The second clade has a broader distribution including southern South America, South Georgia, South Shetland Islands, and the Antarctic Peninsula. The ABC method identified long-distance dispersal (LDD) colonization event(s) from southern South America to South Georgia and the maritime Antarctic after the LGM deglaciation, supporting more recent colonization of Antarctic locations. The current Antarctic and sub-Antarctic distribution of B. poppei is likely derived from two independent biogeographic events. The combination of both (1) post-LGM colonization from southern South America and (2) longer-term persistence in in situ regional refugia throughout glacial periods challenges current understanding of the biogeographic history of Antarctic freshwater biota. Re-colonization of ice-impacted Antarctic areas would have occurred following a LDD and Establishment model, pointing to the existence of possible post-dispersal barriers, despite widely assumed high passive dispersal capacity in freshwater invertebrates.

Cryptic diversity and speciation in an endemic copepod crustacean Harpacticella inopinata within Lake Baikal

“…They are also related to the general observation of 'apparent acceleration of molecular rates' in recent populations (e.g. Crandall et al, 2012;Maturana et al, 2022). Whatever the time scale and rates have been, a difference between the two widespread species that deserves attention is that the expansion peak appears two times older in H. inopinata CE than H. inopinata CW, and if rates were the same this would imply a clearly earlier spread along the eastern shore.…”

“…The patterns in mitochondrial haplotype variation, interpreted as reflecting population size history, varied clearly among the five taxa (Figures 1b and 3; Table 2). The two common ones H. inopinata CE and H. inopinata CW both showed shallow genealogies and star‐like haplotype networks, patterns expected from a relatively rapid demographic expansion following a bottleneck phase (Maturana et al., 2022). It seems that the current populations of the two species, or at least their mitochondria, each trace back to a (local) ancestral population, from which their genes have spread through their current ranges ‘relatively recently’.…”

Freshwater invertebrates from Livingston and Horseshoe Islands, Maritime Antarctica

“…Various adaptations make B. poppei the ultimate coloniser in Antarctic lakes, e.g. protective colouration [17,18]; resting eggs that can survive >100 years [19]; well-functioning pathways of distribution [9,20]. We provide new distributional records for this calanoid species for 19 of the studied lakes and ponds.…”