Published this month we present a chapter on glacial refuges of Antarctic terrestrial biodiversity in the book "Past Antarctica: Paleoclimatology and Climate Change".
Biological research over the last decades has revealed that many of Antarctica's terrestrial biota are endemic to the continent, with nearly every group (invertebrates, microbes, plants) including species which show signals of Antarctic survival on multi-million-year timescales. Some species even show evidence that their Antarctic presence pre-dates the final breakup of Gondwana and the geographic isolation of Antarctica.
For terrestrial life to have existed continuously on the continent over these timescales, appropriate ice-free land must have existed through the multiple glacial cycles that took place throughout the Miocene, Pliocene and Pleistocene eras. In the new chapter, we discuss the evolutionary history of terrestrial life in Antarctica, evidence from glacial reconstructions, as well as the requirement for refugia across all biogeographical regions of Antarctica. We also discuss the likely form that such refugia may have taken, from nunataks, geothermal areas, glacier surfaces, subglacial habitats and cryptobiosis.
For more information see:
Convey, P., Biersma, E.M., Casanova-Katny, A., Maturana, C.S. (2020) Chapter 13: Refuges of Antarctic Biodiversity. In: "Past Antarctica" (ed. J.R. Fernandez). https://doi.org/10.1016/B978-0-12-817925-3.00010-0
The evolution of globally occurring microorganisms is highly driven by dispersal and speciation in isolation
Many microorganism species can be found all across the globe. Their seemingly global distributions have long caused a debate whether microorganisms can disperse very easily and geographic barriers have any effect on them, or whether it has taken them a long time to get everywhere.
Trying to answer that question, a new large-scale genetic study in Nature Communications revealed how a single-celled alga has spread across the globe and in its journey radiated into an unprecedented species diversity since the Eocene/Oligocene global cooling period. In contrast to previous beliefs, it hereby shows that the evolution of microorganisms is highly driven by colonisation to suitable habitats and subsequent speciation in isolation. Although this has long been recognised as a driving force for speciation in larger organisms, it is now also shown to be an important force for speciation in microbial species.
Microbial biogeography: putting the distribution of a global microbe on the map
Many microbial species, i.e. protists, bacteria, archaea and fungi, often have very similar appearances in various corners of the globe. It is therefore generally thought that they lack the biogeographic structure and the clear speciation patterns found in larger organisms. Instead, their supposedly high dispersal rates and large population sizes have long led to the assumption that many microorganisms have global geographic distributions.
To investigate this, Pinseel et al. (2020) studied the evolutionary history of a globally occurring terrestrial diatom species, Pinnularia borealis - a small type of single-celled algae living in terrestrial habitats such as soils and mosses. Sampling >1500 environmental samples across the globe containing >800 strains, the study looked into morphological and genetic analyses to study the species’ evolutionary history, and the timescale on which this small diatom managed to cover most of the planet’s far-flung corners of the globe.
The analyses, however, also suggested that, despite P. borealis being a small, microscopic algae, has been quite good at dispersing. For example, the analyses revealed that all continents had been colonised multiple independent times. In particular, it was surprising that the sub-Antarctic and Antarctic, though highly isolated places, were colonised at least eight independent times, and in several cases through long-distance dispersal from the Northern Hemisphere.
Timing of species diversification and the transition to open terrestrial habitats
Luckily, diatoms have a very good fossil record, and species diversity can be quite accurately calculated over time. Using fossil evidence and genetic dating techniques the radiation of the diatom across the globe was found to have originated since the Eocene/Oligocene boundary (25.0–36.1 million years ago). This period was characterised by a profound change in climate, as the Earth shifted from a greenhouse to an icehouse state, and known as a time of large-scale extinction and floral and faunal turnover. The period, associated with colder and drier climates, also marks the onset of a global expansion of open terrestrial landscapes, in which P. borealis currently thrives.
Time-calibrated species tree of the P. borealis complex. Coloured bars next to the phylogeny indicate the biogeographic region(s) of each species: dark blue: Arctic zone; light blue: boreal zone; purple North America (excl. Arctic); grey: Madagascar; pink: South America; orange: Australasia; yellow: sub-Antarctic; dark red: Antarctic. In the middle-left: species accumulation curve showing the sample-based interpolation (rarefaction) and extrapolation of the P. borealis species delimited in this study. Below: raw (blue) and smoothed (black) oxygen-isotope data reflecting changes in global temperature and continental ice-sheet volume, overlaid with a "lineage-through-time plot" (semi-logarithmic scale) of the P. borealis complex.
How many times would one need to sample to get all extant diversity?
Indeed, despite that over 1500 samples were obtained, the large global sampling effort was still not nearly enough to capture al the diversity within P. borealis. Extrapolation analyses, investigating how the number of species increases with the number of added samples, suggested that that nearly ten thousand environmental samples would need to be gathered all across the globe to find the majority of lineages of just this species complex alone. This means that, at that point one will likely have found most of the global diversity that exists within P. borealis, which was estimated to equal about 415 species. This species diversity far exceeded previous estimates for a diatom lineage of this age (since the Eocene/Oligocene boundary). The high diversity within this species complex alone reflects the likely hidden diversity of other groups of the ‘rare biosphere’.
Implications for general understanding of drivers shaping microbial biogeography
All in all, the new study reveals how ‘rare biosphere’ taxa, which are key players in the global carbon and nutrient cycles, are composed of astonishingly high levels of diversity across the globe. It reveals, contrary to long-held views, how dispersal and subsequent evolution in isolation plays a large role in the evolution of small micro-organisms. The evolutionary history of this one, seemingly insignificant, microscopic algae, illuminates the hidden diversity within the world of small microscopic life, which we still know so little about.
For more information see:
Pinseel, E., Janssens, S.B., Verleyen, E., Vanormelingen, P., Kohler, T.J., Biersma, E.M., Sabbe, K., Van de Vijver, B. & Vyverman, W. (2020) Global radiation in a rare biosphere soil diatom. Nature Communications 11, 2382. https://doi.org/10.1038/s41467-020-16181-0
Multiple late-Pleistocene dispersal events of the Antarctic pearlwort Colobanthus quitensis (Caryophyllaceae) reveal a recent arrival of native Antarctic vascular flora
Antarctica's isolated and extreme terrestrial environments are inhabited by only two species of native vascular flora: the Antarctic pearlwort Colobanthus quitensis (Caryophyllaceae) and the Antarctic hair grass Deschampsia antarctica (Poaceae). While many other groups of terrestrial biota (e.g. mites, springtails, mosses) include species with a long-term (million-year) survival and high endemism in Antarctica, the age and origin of both vascular plants was until now not yet thoroughly studied.
A new paper in Journal of Biogeography on the Antarctic pearlwort C. quitensis (shown in Fig. 1), completing previous biogeographic assessments of the Antarctic hair grass, shows that the vascular flora of Antarctica is of likely late-Pleistocene origin. The vascular flora is hereby the first identified group of terrestrial organisms to be completely of recent arrival, with a likely origin after major glacial periods in Antartica.
The overall findings of multiple colonisation events by a vascular plant species to Antarctica, and the recent timing of these events, are of also significance with respect to future colonisations of the Antarctic by vascular plants, particularly with predicted increases in ice-free land in the Antarctic Peninsula. The results also suggest the Antarctic is less isolated for this species than previously thought.
Fig. 3. Genotype and haplotype networks of Colobanthus quitensis based on nuclear (a) and chloroplast (b, e, f) markers, and nuclear and chloroplast regions combined (c). Map (d) showing sample locations of the two Maritime Antarctic haplotype groups identified in (c) (indicated in with dashed ellipses). Colours of different biogeographic regions are shown in the key.
Late-Pleistocene origin of vascular flora - a contrasting pattern to many other terrestrial biota
During the Last Glacial Maximum, as well as during previous glaciation periods, almost the entire continent of Antarctica is thought to have been covered by ice. The general assumption has therefore long been that basically no terrestrial life could have persisted in Antarctica throughout this time, and all life must be of recent (post-glacial) origin.
Recent biological research has challenged this view, revealing many examples of species with long-term pre-glacial persistence, suggesting that life must have persisted throughout previous glaciation periods in the Antarctic. Evidence can be found in almost every group of terrestrial organisms (e.g. nematode worms, diatoms, springtails, insects, mosses etc), with timespans of isolation in Antarctica ranging from hundreds of thousands to millions of years. Some groups even show ages of isolation since the break-up of ‘Gondwana’, where Antarctica broke off from the other Southern Hemisphere continents.
Antarctica only continent with a recent (thousand year-scale) vascular flora
In the new study on the cushion plant Colobanthus quitensis we find that the Antarctic populations of the species likely derived from two independent, late-Pleistocene dispersal events. Adding to previous inferences on the other Antarctic vascular plant species (a grass called Deschampsia antarctica), we suggest that both vascular plant species are likely to have arrived on a recent (late-Pleistocene) timescale. Contrary to the other groups of terrestrial biota, the vascular flora stands out as the first identified terrestrial group that appears to be entirely of recent origin.
For more information see:
Biersma, E.M., Torres-Díaz, C., Molina-Montenegro, M.A., Newsham, K.K., Vidal, M.A., Collado G.A., Acuña-Rodríguez, I.S., Ballesteros, G., Figueroa, C.C., Goodall-Copestake, W.P., Leppe, M.A., Cuba-Díaz, M., Valladares, M.A., Pertierra, L.R. & Convey, P. (2020) Multiple post-glacial colonisation events of the Antarctic pearlwort Colobanthus quitensis (Caryophyllaceae) reveal the recent arrival of native Antarctic vascular flora. Journal of Biogeography
Different from previous fieldwork, this year Bo Elberling, his daughter and I joined a tourist ship (Albatros Expeditions). We took samples and measurements at each penguin colony, while giving guests hands-on experience on how scientific studies are conducted and how data are collected in the field (citizen science). It was a great success, and we got measurements done at all three common penguin colonies at the Antarctic Peninsula (Gentoo, Adelie and Chinstrap penguins). We also gave several presentations onboard the ship on topics related to climate change, marine and terrestrial biology, conservation and biogeography with a specific focus on the polar regions, which led to engaging discussions and interactions with the guests.
Bo Elberling and his daughter taking gas samples at the Gentoo penguin colony at Port Lockroy
The combined influence of glacial retreat and penguin guano on soil greenhouse gas fluxes in South Georgia
A new paper revealed the combined effects of glacial retreat and fertilisation by King Penguins on soil greenhouse gas fluxes on the soil succession at St. Andrews Bay, South Georgia; the largest King Penguin colony in the world (~150,000 breeding pairs). The production and consumption of three greenhouse gasses (CO2, CH4 and N2O) were assessed based on laboratory incubations of soil cores, as well as incubation experiments with added nutrients and water.
We found that soils located at a greater distance from the retreating glacier front showed a successive development, with expanding vegetation cover and increasing soil nutrient content, coinciding with increased CO2 production and CH4 consumption rates. Towards sites with an increase in penguin activity and guano deposition, the CO2 production increased by 4–16-fold while the CH4 consumption decreased by about half. N2O production rates were not affected by exposure time since glacial retreat, but increased markedly (approximately 120-fold) at the site with the highest penguin activity. Along the transect, labile C and moisture were considered the key limiting factors for CO2 production, while moisture likely explain the limitation of CH4 consumption.
For more information see:
Wang P., D'Imperio L., Biersma E.M., Ranniku R., Xu W., Tian Q., Ambus P., Elberling B. (2019). Combined effects of glacial retreat and penguin activity on soil greenhouse gas fluxes on South Georgia, sub-Antarctica. Science of the Total Environment, 135255.
This last part of August was spent on fieldwork in the region of Kangerlussuaq (Søndre Strømfjord) in western Greenland to sample plants for my future postdoctoral project on finding out more on the evolutionary history of the Greenlandic flora.
The aim of this project is to study the routes and timings of floral colonisation into and within Greenland to place Arctic floral biogeography more firmly into the contexts of the northern landmasses and the glaciation history of Greenland itself. In addition, I hope to gain a better understanding of speciation processes of plants in polar regions (e.g. effects of past climate, bottlenecks, asexual reproduction, polyploidy and hybridisation). For this project I will use a combination of fresh and herbarium material, combined with population genetic and molecular dating methods.
The project will be based at the Natural History Museum of Denmark and the University of Copenhagen, and is funded by the Carlsberg Foundation.
The project will start part-time and in the meanwhile I will continue to work at the British Antarctic Survey as well.
This December I joined Stef Bokhorst for a fieldwork trip in Navarino Island in the Cape Horn region in southern Chile, to study the effect of invasive species in the Antarctic and sub-Antarctic.
We set up several sets of long-term experiments on the mountain top near Puerto Williams, as this experimental side showed a lot of similarities with the type of fellfield habitat you can find in many parts of the Maritime Antarctic.
The experiments were designed to study the effect of new species on the growth of the native Antarctic flora, as well as disentangling possible elements which may be of importance to future establisment of invasive species, e.g. the effects of water-retention in the native species on the establishment of new species, or what species may enhance or inhibit each others presence.
It was a busy but productive trip, and great to be back in the beautiful Beagle Channel area! Many thanks to Stef for inviting me to be part of this fieldwork, and thanks to Tamara Contador, Roy Mackenzie and others from the Puerto Williams Biological Field Station for help with the work!
From 13-16 August 2018 about 25 terrestrial scientists gathered in Ny-Ålesund for the Terrestrial Flagship Meeting, funded by the Svalbard Science Forum. The aim of the workshop was to increase cooperation in measurements, data use, publications, study sites and experimental manipulations amongst terrestrial scientists studying tundra or lakes in the Ny-Ålesund/Kongsfjord area.
It was a very fruitful meeting, with many interesting conversations and possible new collaborations... and hopefully resulting in a review paper from the terrestrial science happening in what is probably the most intensely studied area in the Arctic!
In July 17-27 Dr. Kevin Newsham and I visited the Arctic Station on Disko Island on Western Greenland, where we studied plant root colonisation by fungi. We studied the effect of habitat wetness (swampy conditions or on top of hummocks) and the effect of winter snow conditions on the amount of fungi present in the roots. We will soon conduct additional labwork on nutrient transfer by fungi into the plant roots.
Below some pictures of the field- and lab-work. Hopefully more results to show soon!
Methane oxidation in soils from sub-Antarctic South Georgia Island
Two multidisciplinary Master thesis projects are proposed and can be initiated as soon as possible. We seek students with a key interest in cold region biogeochemistry including greenhouse gas fluxes and in microbial ecology and molecular analyses of bacterial communities. The project is a collaboration project between British Antarctic Survey (BAS) and University of Copenhagen/Center for Permafrost (CENPERM).
See the announcement here: https://cenperm.ku.dk/news/msc-projects-announcement/
Many computer models describing high latitude carbon (C) dynamics have focused on wetland areas, as they form the largest source of the greenhouse gas methane (CH4) and may therefore act as a positive climate feedback mechanism. However, the role of dry ecosystem types, such as upland mineral soils and polar deserts, in the global C budget is often overlooked despite that such habitats dominate the high latitude regions. Recent laboratory and field studies show that high latitude dry ice-free ecosystems act as a substantial CH4 sink due to the presence and activity of bacterial communities oxidizing atmospheric CH4 at high rates. Furthermore, it has been observed that CH4 oxidation rates may increase with increasing air temperature. Improved knowledge on the rates, drivers and spatial distribution of CH4 oxidation in high latitude areas is now critical for optimizing, parameterizing and validating mechanistic and climatic models, which help to predict global present and future climate scenarios.
We are interested in testing the CH4 oxidation potential of upland mineral soil from sub-Antarctic South Georgia Island under controlled conditions in the laboratory (e.g.different climatic conditions and nutrient levels) and relate the measured C (CH4 and carbon dioxide (CO2)) fluxes to the soil type and microbial community at the site. The microbial community will be assessed using Next Generation Sequencing (NGS) of 16S rRNA gene amplicons (a marker used for identifying bacterial and archaeal diversity), fungal ITS2 amplicons, and possibly of the pmoA gene, which is a marker for CH4-oxidizing bacteria. Soil samples have been collected during the austral summer 2017/2018 on South Georgia Island. The site has been chosen based on field measurements, which showed very high CH4 oxidation rates comparable to those measured in upland Arctic and temperate soil ecosystems. The results will contribute to a larger project, which will include observations from Svalbard and Greenland, in order to better understand and upscale the spatial distribution of atmospheric CH4 oxidation at high latitude areas. It will also improve the knowledge of the distribution of the microbial communities involved in methane oxidation.
We are looking for two motivated candidates, who are interested in carrying out soil incubations experiments and molecular laboratory techniques. Soil incubations will take place at CENPERM, while molecular work will take place at the Section of Microbiology, Department of Biology, both situated at University of Copenhagen.
If you are mainly interested in molecular laboratory techniques:
Elise Biersma firstname.lastname@example.org or Anders Priemé email@example.com
or if you are mainly interested in soil incubations:
Ludovica D'Imperio firstname.lastname@example.org or Bo Elberling email@example.com
Molecular Data Suggest Long-Term in Situ Antarctic Persistence Within Antarctica’s Most Speciose Plant Genus: Schistidium
Schistidium reveals an old evolutionary history on the continent
In a recent phylogenetic study we assessed the diversity, richness and relative age divergences within the moss genus Schistidium (Fig. 1). It is the most species-rich plant genus in the Antarctic, as well as the plant genus containing most Antarctic endemic species. It is therefore a particularly interesting genus to investigate for possible long-term in situ persistence.
The phylogenetic analyses revealed that most previously described Antarctic Schistidium species were genetically distinct, confirming the validity of at least seven of the thirteen currently recognized Antarctic species. The molecular dating analyses suggested that all divergences between species took place at least ~1 Mya, suggesting a likely in situ persistence in Antarctica for (at least) all endemic Schistidium species (Fig. 2). This provides a valuable contribution to studies on the adaptive potential of Antarctic plants to survive climate change (throughout both warmer and colder conditions) over both historical and contemporary timescales.
Fig. 2. Molecular dating analyses showing a phylogenetic tree with estimated divergence times between and within different Antarctic Schistidium species.Timescales for different rates are shown and are based on previously calculated nuclear substitution rate from (a) Polytrichaceae mosses, and (b) flowering plants. For more information see here.
The endemic species Schistidium antarctici: a common and particularly old Antarctic plant species
Schistidium antarctici, one of the most widespread and abundant moss species in Antarctica, can be found in nearly all ice-free coastal regions of all generally accepted Antarctic sectors. The molecular analyses (Fig. 2; above) suggest that the species diverged from other Antarctic species in the late Miocene, thereby revealing the oldest extant plant species currently known in Antarctica.
In a population genetic analysis of the species (Fig. 3, below) we could identify several distinct clades, dividing the eastern Antarctic Peninsula and Scotia Arc islands (South Orkney Islands, South Georgia) from the western Antarctic Peninsula and all continental locations.
Fig. 3. Locations of different haplotypes within Schistidium antarctici in the Antarctic and sub-Antarctic. (B) shows a more detailed map of the northern maritime Antarctic. A haplotype network is presented in (C), including the number of individuals per haplotype. For more information see here.
The analyses reveal several interesting findings. Firstly, the populations of the Antarctic continent are genetically very similar and appear to have been derived from only one haplotype (haplotype 2, Fig. 3), which likely spread from the Peninsula area to the rest of the continent.
Secondly, the highest genetic variation was found in the northern Antarctic Peninsula region, suggesting that this is likely a region where the species survived the throughout glacial cycles in situ.
And lastly, the analyses suggest that the mountainous spine on the Antarctic Peninsula appears to form a barrier to gene flow (Fig. 3B), a division also seen in other terrestrial groups (e.g. rotifers and diatoms). This suggests the existence of distinct bioregions on either side. This finding has implications for conservation priorities, suggesting an increased protection of the vegetation of the north-east Antarctic Peninsula may be needed.
Fig. 4. A 'lush' area in the South Shetland Islands in the northern maritime Antarctic.
Biersma E.M., Jackson, J.A., Stech, M., Griffiths, H., Linse, K. & Convey, P. (2018) Molecular data suggest long-term in situ Antarctic persistence within Antarctica's most speciose plant genus, Schistidium. Frontiers in Ecology and Evolution. 6, 77.
Despite extreme survival abilities, the moss Chorisodontium aciphyllum is a likely recent arrival in Antarctica
The connectivity and origin of the contemporary Antarctic biota have become central questions in Antarctic biogeographic studies. A new population genetic study on the moss Chorisodontium aciphyllum, known for its extreme revival abilities as well as having the oldest sub-fossils of any extant plant in Antarctica, revealed no to very low genetic variation between South American and Antarctic populations, suggesting a likely recent (<1 million year) arrival in the Antarctic. This is in contrast with many other species of Antarctica’s extant terrestrial biota, which are estimated to have been isolated in situ on much longer timescales.
Old sub-fossils and extreme survival abilities
The bank-forming moss Chorisodontium aciphyllum is a pretty extreme plant. The moss occurs in southern South America and into the maritime Antarctic, where it grows to form deep (~1-3 m) moss banks. These peat banks are known to be the oldest sub-fossils of any extant plant in Antarctica; the bases of 1.5 m deep peat banks have been radiocarbon dated at ~5000-5500 years old, and deeper cores may potentially be much older. The peat is also a valuable resource for reconstructing past climate, providing useful data on past moisture and temperature in the maritime Antarctic.
Low genetic variation suggests likely recent (<1 Myr) Antarctic arrival
The extreme survival abilities together with the old sub-fossils make C. aciphyllum a particularly interesting species to study for possible long-term survival in Antarctica - i.e. longer than the Last Glacial Maximum (~18-20 kya). However, applying phylogeographic and population genetic methods to both chloroplast and nuclear loci revealed no to very low genetic variation within C. aciphyllum throughout it's range, both between and within Antarctic and southern South American populations (see figure below). This suggests that the plant has been in the Antarctic for a relatively short amount of time, as the populations haven't been separated for long enough to accumulate mutations.
Bayesian phylogenetic trees and haplotype networks constructed with plastid (a-b) and nuclear (c) loci reveal no to very little genetic variation between and within Antarctic and southern South American populations of Chorisodontium aciphyllum. For details see study.
Exactly how long the species has been present in the Antarctic is uncertain. However, theoretically, applying a simplistic calculation from a predefined substitution rate we would expect one substitution to have happened at least every ~1 Myr in the fastest evolving studied locus. This suggests populations in South America and the Antarctic have likely been separated no longer than one million years, and a minimum of ~5.5 ky, the age of the oldest dated Antarctic C. aciphyllum peat core. It should be noted that this is a very rough calculation due to various difficulties of molecular dating with bryophytes (e.g. lack of fossils and complication of relying mostly on asexual/clonal reproduction).
Antarctic may be less isolated for spore-dispersed organisms than previously thought
In order to further assess the connectivity of small or spore-dispersed organisms between South America and Antarctica, we modeled the relative frequency and direction of atmospheric transfer events between the regions. These analyses show that small particles transported via regional air masses can clearly cover long distances within a 24 h period (see figures below). The results also reveal a strong asymmetry in directional probability, showing that aerial transfer from southern South America to the northern maritime Antarctic (a) is more likely than vice versa (b). The results show the clear influence of the westerly winds prevailing in the region, and that west-to-east transport is much more likely than east-to-west - and that getting to the Antarctic from South America is easier than the other way around.
Dispersal density spatial maps expressed as the percentage of times that an air mass from a given initial location passes within a radius of 200 km, re-created from daily air mass movements within a 24-h period. a and b represent starting locations (shown as asterisks) from southern South America and the northern maritime Antarctic, respectively. For details see study.
Biersma E.M., Jackson, J.A., Bracegirdle T.J., Griffiths, H., Linse, K. & Convey, P. (2018) Low genetic variation between South American and Antarctic populations of the bank-forming moss Chorisodontium aciphyllum (Dicranaceae). Polar Biology, 1-12. https://doi.org/10.1007/s00300-017-2221-1
Hi! I am Elise Biersma, an evolutionary biologist studying polar plants and microbes.