Antarctic lichens with different population history show grossly diverging genetic patterns.
Above: Antarctic lichens (Usnea) near Carlini station on King George Island, January 2016 (Elisa Lagostina).
The Antarctic is arguably the most remote place on Earth and difficult to reach for scientists and other organisms. In many people’s imagination it may just be a vast ice dome with scattered penguins along its margins. But in fact, it harbours isolated pockets of seasonally ice-free terrain with an amazing diversity of life. For lichenologists like us, Antarctica is a special place, because for once our favourites are not marginalized by vascular plants. They absolutely dominate the terrestrial landscape, as the photo above illustrates. This is of course due to the extreme environmental conditions, most of all low temperatures and a short vegetation period, which affect lichens to a much lesser degree than flowering plants. Lichens are symbioses between fungi and photosynthetic organisms. Most species can photosynthesize without liquid water when air humidity is high enough, some even at sub-zero temperatures. And when conditions get really tough, they can dry out completely and persist in a state of latent life.
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Lagostina, E., Andreev, M., Dal Grande, F., Grewe, F., Lorenz, A., Lumbsch, H.T., Rozzi, R., Ruprecht, U., Sancho, L.G., Søchting, U., Scur, M., Wirtz, N. and Printzen, C. (2021). Effects of dispersal strategy and migration history on genetic diversity and population structure of Antarctic lichens. J Biogeogr. 48:1635–1653. https://doi.org/10.1111/jbi.14101
Although Antarctica is the continent least affected by humans, it is no longer a pristine environment. Antarctic ecosystems are particularly threatened by global warming and ever increasing numbers of human visitors, both of which interact to increase the risk of invasive species being introduced. It is here that our project started. Most lichens have particularly wide distributional ranges. For example, the most common lichens of the Maritime Antarctic, Usnea antarctica and U. aurantiacoatra, had both been reported from southern South America as well. What seems to be good news at first view – the species are obviously able to cope with milder climatic conditions – could actually turn into a severe conservational threat, if warm-adapted genotypes from South America got a chance to outcompete their cold-adapted Antarctic neighbors. After all, the convention on biological diversity explicitly mentions genetic diversity as one of the fundamental elements of biodiversity.
Usnea antarctica on a stone on King George Island, the asexual species spread with
soredia visible on the thallus. (Photograph by Elisa Lagostina.)
When we started this project, nothing was known about the genetic structure of Antarctic lichen populations or the extent of genetic exchange between isolated Antarctic regions and southern South America. In order to change this, we had to overcome two major obstacles. Sampling for population genetic projects in the terrestrial Antarctic is a nightmare, particularly within the framework of short-term projects. If you are lucky to get space on one of the few Antarctic research stations, you are basically stuck within a radius of at most 10-20 km and no chance to get access to any other station before the next season. The only workaround is to involve as many other lichenologists as possible into your project. We were extremely lucky that Austrian, Brazilian, Danish, Russian, and Spanish colleagues were more than willing to contribute to the sampling and managed to get their own projects funded.
The second obstacle was of a technical nature. Lichens are known to evolve slowly. DNA sequences usually show few differences and very rarely clear geographic patterns. We therefore decided to use SSR markers, which first had to be developed from newly assembled draft genomes. Designing the primers along genomic sequences of two closely related species offered the first nice surprise in this project: our more than 20 markers amplified extremely reliably and across species boundaries. In the end we had a data set almost without any gaps (“null alleles”). And because we were able to amplify the exact same loci in the two Usnea species, we could show once and for all that they were not conspecific as some (including the older one of us) had once assumed in the past.
Usnea aurantiacoatra on the ground in King George Island, the sexual species
has big black Apothecia visible on the thallus. (Photograph by Elisa Lagostina.)
The third difficulty is typical for lichen studies but nevertheless caught us entirely unprepared. We had planned to study the two Usnea species along with two crustose lichens from the genus Placopsis to account for possible differences in growth form and reproductive mode. Usnea aurantiacoatra and Placopsis contortuplicata (lichenologists have a deeply rooted desire to create unpronounceable scientific names) reproduce sexually by ascospores, while Usnea antarctica and Placopsis antarctica use vegetative propagules, so-called soredia, to disperse both symbionts together. These four species are big and showy (for lichen standards) and had been reported from both sides of the Drake Passage. To our bewilderment, none of the U. antarctica look-alikes sampled in South America actually belonged to this species. Genetically, they all proved to be stunted forms of U. aurantiacoatra or its near relative U. trachycarpa. Apparently, the species had been wrongly reported from South America and is in fact an Antarctic endemic. Worse, we could not find the Placopsis species either. We decided to make a virtue out of necessity and adjusted our original sampling strategy to include Cetraria aculeata as an example of an asexually reproducing species. We had previously studied this species in various parts of the world including South America and the Antarctic and knew that it was disjunct between both continents. Moreover, we knew that it had colonized the Southern Hemisphere from the north in contrast to U. aurantiacoatra, which is not known further north than southern Chile and Argentina. This not only allowed us to assess the impact of phylogeographic history on regional patterns of genetic diversity but ultimately resulted in the detection of a crystal clear geographic pattern of genetic diversification and a more precise dating of a colonization event. The latter, by the way was also due to a reviewer nudging us to apply Approximate Bayesian Computation to compare different phylogeographic scenarios for our species.
We found evidence for glacial in situ survival of Usnea aurantiacoatra in South America and in the Antarctic, where also Usnea antarctica displays its highest diversity. Cetraria aculeata, on the other hand, colonized the Antarctic only after the Last Glacial Maximum from South America in at least three independent events. The good result for the Antarctic conservation is that we found no convincing evidence for ongoing gene flow from southern South America into the Maritime Antarctic. Nevertheless, maintaining the strong genetic differentiation of Antarctic populations of Cetraria aculeata requires strict conservation measures, whereas populations of Usnea aurantiacoatra are exposed to a much lower risk due to their higher diversity and connectivity.
So far our studies were focused entirely on the fungal partner of the symbiosis. One obvious way to proceed in the future is to study the algal partners of our species to see whether association with genetically different strands helps them to adapt to different ecological conditions. We already know that lichens can associate with genetically different partners and that lichen photobionts are shared among different species in the same habitat (“lichen guilds”). The implications of these phenomena must be very different in vegetatively and sexually reproducing species. This is another field, which has virtually not been studied in Antarctica and where we are almost certain to meet with surprising results. Grant reviewers, unfortunately, have so far not swallowed the bait. But as long as the Western Antarctic Ice Shield has not collapsed there is hope!
Cetraria aculeata from Bale Mts., Ethiopia.
(Photograph by Christian Printzen.)
Elisa Lagostina, PhD
Christian Printzen, Head of Cryptogams Section
Department of Botany and Molecular Evolution, Senckenberg Research Institute and Natural History Museum Frankfurt, Frankfurt/Main, Germany.