Introduction
Antarctica's terrestrial ecosystems are home to thriving populations of soil invertebrates (Chown & Convey Reference Chown and Convey2016) that inhabit the seasonally snow- and ice-free soils (Chown & Convey Reference Chown and Convey2007). To date, some 550 species of Antarctic invertebrates have been described, with 170 of these being endemic to the region (Adams et al. Reference Adams, Wall, Virginia, Broos and Knox2014, Velasco-Castrillón et al. Reference Velasco-Castrillón, Gibson and Stevens2014a). Morphology-based taxonomy has advanced the study of their biodiversity and distribution (Nielsen Reference Nielsen2019). However, confirming these patterns for all Antarctic taxa has been constrained by the region's limited accessibility (Convey Reference Convey2011, Chown et al. Reference Chown, Clarke, Fraser, Cary, Moon and McGeoch2015) and the demanding taxonomic expertise required for microinvertebrate identification. Molecular approaches are now revealing profound insights into the origin, diversity and distribution of terrestrial Antarctic invertebrates, confirming certain aspects, such as climatic bioregions (e.g. Maritime and Continental Antarctica; Pugh & Convey Reference Pugh and Convey2008), and a consensus has formed regarding the ancient origins and complex evolutionary history of Antarctica's invertebrate biota (Marshall & Pugh Reference Marshall and Pugh.1996, McInnes & Pugh Reference McInnes and Pugh1998), despite early speculation of there having been recent colonization (Starý & Block Reference Starý and Block1998).
Phylogeographic analysis is a powerful tool that can generate and test theories of evolutionary timelines from sequence alignments and provide statistical rigour to the evaluation of events important to species distributions. The combination of sequencing data with biogeographical histories can detail both recent and ancient ancestries. Most phylogeographic studies focus on Northern Hemisphere taxa (Beheregaray Reference Beheregaray2008), but a growing number of studies have targeted invertebrates from the Antarctic region. Here we review published phylogeographic studies of Antarctic soil fauna within its three constituent regions, each with distinct climatic and geological histories: 1) Continental Antarctica, 2) Maritime Antarctica and 3) the sub-Antarctic islands (Fig. 1). First, we introduce the geological and climatic histories that have shaped both the region and its terrestrial fauna, before providing a brief overview of the main phylogeographic approaches. We then summarize the general patterns found within and among the regions for the dominant invertebrate groups, specifically mites (Acari), springtails (Collembola), nematodes (Nematoda), rotifers (Rotifera), tardigrades (Tardigrada) and the chironomid midges (Chironomidae). Some examples of each group include the oribatid mites Halozetes belgicae Michael, 1903 and Membranoppia loxolineata Wallwork, 1965, the springtail Cryptopygus cisantarcticus Willem, 1901, the nematode Scottnema lindsayae Timm, 1971, the rotifer Macrotrachela jankoi Iakovenko, Reference Iakovenko, Smykla, Convey, Kašparová, Kozeretska and Trokhymets2015 and the tardigrade Hypsibius exemplaris Doyère, 1840 (Fig. 2). While the Protozoa are considered to be soil fauna, as a subkingdom of the Protista, they are more commonly associated with marine habitats and there are few morphological and molecular records of these in Antarctic soils (Smith Reference Smith1996, Lawley et al. Reference Lawley, Ripley, Bridge and Convey2004, Thompson Reference Thompson2021). We therefore focus on other non-microbial taxa that are found predominantly in terrestrial systems. Finally, we focus on the future directions for terrestrial Antarctic invertebrate research and evaluate the capacity to monitor and protect the unique Antarctic ecosystems.
Figure 1. Map of the three Antarctic regions: continental, maritime and sub-Antarctic islands (source: Google Earth image based on Landsat and Copernicus satellite images, Maxar Technologies). Overlay of the circumpolar distributions of sequenced springtail specimens (yellow triangles) and other invertebrates (blue circles; adapted from McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011). Red boxes outlining Victoria Land and Graham Land are detailed in Fig. 4a,b.
Figure 2. Photographs of the main groups of Antarctic soil fauna: a. oribatid mites Halozetes antarcticus and Oppia loxolineata (source: GMR), b. springtail Cryptopygus cisantarcticus (source: GMR), c. nematode Scottnema Lindsayae (source: Barcode of Life Data System (BOLD), uncredited), d. rotifer Macrotrachela jankoi (source: Iakovenko Reference Iakovenko, Smykla, Convey, Kašparová, Kozeretska and Trokhymets2015; NERC Open Access Research Archive (NORA), http://nora.nerc.ac.uk/) and e. tardigrade Hypsibius exemplaris (source: Jönsson Reference Jönsson2019).
Geological history
Antarctica's current landmass and geological features have been well described (Convey et al. Reference Convey, Bowman, Chown, Francis, Fraser, Smellie, Hoorn, Perrigo and Antonelli2018), and they were historically part of the early supercontinent Rodinia that existed between 1300 and 700 million years ago (Ma; Fuck et al. Reference Fuck, Neves and Schobbenhaus2008). This protocontinent underwent separation and reformed as Pangea, which itself began breaking up ~335 Ma. The rifted supercontinent of Laurasia encompassed the North American, European and Asian continents. Meanwhile, the southerly Gondwanan portion contained the Antarctic, South American, African and Australian continents (McMenamin & McMenamin Reference McMenamin and McMenamin1990). As Pangea separated, Antarctica was already positioned over the South Pole (Rogers & Santosh Reference Rogers and Santosh2004), but it then supported lush forests and a thriving dinosaur population (Rozadilla et al. 2015). Gondwana began to break up ~175 Ma, with Australia and South America beginning to separate 85–60 Ma, before moving swiftly northwards by 35 Ma. These final movements created the channels on either side of the Antarctic continent (Wei Reference Wei2004, Hassold et al. Reference Hassold, Rea, van der Pluijm and Parés2009), allowing the establishment of the Antarctic Circumpolar Current (ACC; Siegert et al. Reference Siegert, Barrett, Deconto, Dunbar, Cofaigh, Passchier and Naish2008). This formed a profound physical barrier and affected the region's climate, limiting biotic crossings and suitable habitat (Pugh & Convey Reference Pugh and Convey2008).
Past and current Antarctic climate
Since Antarctica's separation from Gondwanaland, the climate has gradually cooled, until low temperatures precipitated the southern ice cap by 44 Ma (Ehrmann & Mackensen Reference Ehrmann and Mackensen1992), followed by repeated cycles of glaciation and ablation occurring over the last 2 million years (2 Ma) until the Last Glacial Maximum (LGM; 22–12 thousand years ago (Ka); Davies et al. Reference Davies, Hambrey, Smellie, Carrivick and Glasser2012). During this repeated glaciation, ice sheets covered most of Maritime and Continental Antarctica, reaching a depth of 7 km on the continent. This would have led to the local extinction of most of the indigenous floral and faunal species (Pugh & Convey Reference Pugh and Convey2008). Throughout the Pleistocene (~2.5 Ma–12 Ka), at least eight glacial cycles occurred, with colder temperatures and greater snowfall advancing the ice sheets. The episodic glaciations had a pronounced 100 Ka cycle between the earlier periods (0.74–0.43 Ma; EPICA Community Members 2004), accelerating into a 40 Ka cycle in the last four glaciations starting from 430 Ka (Augustin et al. Reference Augustin, Barbante, Barnes, Barnola, Bigler and Castellano2004). Interglacial periods had more favourable temperatures and greater water availability, allowing terrestrial ecosystems to thrive.
Continental Antarctic temperatures are cold and dry all year round in the high plateaus (mean annual temperature (MAT): -55°C), with milder conditions in coastal regions (MAT: -10°C; Turner et al. Reference Turner, Colwell, Marshall, Lachlan-Cope, Carleton and Jones2005, SOE 2011). Yet summer temperatures and increased solar radiation thaw soils in some regions, facilitating biological activity. In maritime areas, summer temperatures can reach 15°C but generally remain below 0°C, while rainfall is more common at lower altitudes along the Antarctic Peninsula. The maritime region is bounded by the extent of the ice shelves off the western side of the peninsula and the islands below the Antarctic Polar Front. Despite the lower latitudes, the South Shetland and Orkney islands are exposed to strong winds that keep MAT to below -4°C. The sub-Antarctic islands lie above the limit of sea ice, with MAT ~2°C and occasional rain during the summer (Turner et al. Reference Turner, Colwell, Marshall, Lachlan-Cope, Carleton and Jones2005).
Rapid deglaciation in the last century on the peninsula's west coast (Cook et al. 2005, 2016, Çiner et al. Reference Çiner, Yildirim, Sarikaya, Seong and Yu2019) is undoubtedly linked to contemporary increases in temperatures, estimated at local rates of up to 0.56°C every decade in the latter half of the twentieth century (Turner et al. Reference Turner, Colwell, Marshall, Lachlan-Cope, Carleton and Jones2005, Reference Turner, Bindschadler, Convey, Di Prisco, Fahrbach and Gutt2009), with additional pronounced peninsular warming since 2000 (Siegert et al. Reference Siegert, Rumble, Atkinson, Rogelj, Edwards and Davies2019). This has led to accelerated greening of sub-Antarctic islands, with expected increased susceptibility to invasive species (Cannone et al. Reference Cannone, Malfasi, Favero-Longo, Convey and Guglielmin2022). Further local warming associated with the diminishing Antarctic ozone hole (Solomon et al. Reference Solomon, Ivy, Kinnison, Mills, Neely III and Schmidt2016) has been predicted to enhance glacier melt, with a 25% increase in ice-free land along the eastern Continental Antarctic coastline and peninsula predicted by 2100 (Lee et al. Reference Lee, Raymond, Bracegirdle, Chades, Fuller, Shaw and Terauds2017). These climate scenarios are expected to expand habitable areas in the maritime and peninsular regions (Turner et al. Reference Turner, Bindschadler, Convey, Di Prisco, Fahrbach and Gutt2009), with larger ranges of continental species (Barrett et al. Reference Barrett, Virginia, Wall, Cary, Adams, Hacker and Aislabie2006). These changes to vegetation and soil microhabitat may influence the distribution and diversity of native fauna (Wall & Moore Reference Wall and Moore1999) or have to contend with greater colonization rates and competition, reinforcing the need for ecosystem monitoring to inform conservation efforts (Parmesan & Yohe Reference Parmesan and Yohe2003, Nielsen et al. Reference Nielsen, Wall, Li, Toro, Adams and Virginia2011b).
The origins and evolution of Antarctic terrestrial fauna
Early theories regarding invertebrate origins proposed that their diversity was a result of rapid evolution following migration from surrounding oceanic islands or continental landmasses after the LGM via wave or wind dispersal (Starý & Block Reference Starý and Block1998). Pronounced glaciation during the LGM and evidence of accelerated dispersal, colonization and speciation following the LGM supported this theory (Peck et al. Reference Peck, Convey and Barnes2006). Here, the ACC can be seen to precede the majority of species radiation. This may be due to the strong physical barriers caused by the current that have limited colonization events, thereby fostering endemism. It must be noted that while dispersal and vicariance can both occur, and potentially produce similar phylogeographic patterns, detailed analyses of molecular markers are able to define the phylogenetic relatedness between species and determine the most statistically probable history based on calibrated evolutionary models. For example, high divergence among populations of endemic springtail species indicates rapid speciation in situ throughout the pre-Pleistocene (> 3 Ma; Knowles Reference Knowles2001), while certain indigenous mite taxa show molecular evidence of pre-Gondwanan origins (> 32 Ma; Pugh & Convey Reference Pugh and Convey2008). These ancient origins adhere to the idea of Gondwanan vicariance, whereby populations were split apart following the rifting of the supercontinent (Krosch et al. Reference Krosch, Baker, Mather and Cranston2011). Arguments against the theory of ancient origins point to a lack of strong evidence for refugial locations (Fontaneto et al. Reference Fontaneto, Kaya, Herniou and Barraclough2009). However, molecular analyses support the consensus of ancient origins (Pugh & Convey Reference Pugh and Convey2008, Warren et al. Reference Warren, Cardillo, Rosauer and Bolnick2014).
Early climate change refugees
The current consensus is that many of Antarctica's indigenous invertebrates survived through periods of glaciation in situ, relying on suitable refugia to endure the ice ages (Convey et al. Reference Convey, Gibson, Hillenbrand, Hodgson, Pugh, Smellie and Stevens2008, Reference Convey, Biersma, Casanova-Katny, Maturana, Oliva and Fernandez2020, Hawes Reference Hawes2015, Stevens & Mackintosh Reference Stevens and MacKintosh2023). Despite widespread ice-sheet coverage, strong biological and phylogeographical evidence points towards the presence of habitable ice-free areas throughout the past 5 Ma (Prentice et al. Reference Prentice, Sykes, Lautenschlager, Harrison, Denissenko and Bartlein1993, Pugh & Convey Reference Pugh and Convey2008). Such refugia are thought to be associated with geothermal activity, coastal areas, the continental McMurdo Dry Valleys and high-altitude ridges, horns and arêtes, collectively named ‘nunataks’, that lie above the maximum glacial height (Pugh & Convey Reference Pugh and Convey2008, Fraser et al. Reference Fraser, Terauds, Smellie, Convey and Chown2014, Reference Fraser, Connell, Lee and Cary2018). Freshwater lakes and ponds have also been proposed as key invertebrate refugia (Wagner et al. Reference Wagner, Melles, Doran, Kenig, Forman, Pierau and Allen2006) before sea-level rises associated with the LGM inundated these sites with seawater (Squier et al. Reference Squier, Hodgson and Keely2002, Cromer et al. Reference Cromer, Gibson, Swadling and Hodgson2006). However, not all proposed refugial sites may be habitable or ice-free given the discovery of barren, high-elevation, hypersaline sites near the continental Beardmore Glacier (Lyons et al. Reference Lyons, Deuerling, Welch, Welch, Michalski and Walters2016) and the evidence of glaciation at potential refugial sites along the peninsula (Lau et al. Reference Lau, Wilson, Silva and Strugnell2020).
Antarctic invertebrates have adapted to local conditions, allowing them to undergo desiccation (anhydrobiosis) or to enter a state of dormancy to withstand freezing (cryptobiosis). Anhydrobiosis is particularly useful for longer-term survival and is common to Antarctic springtails (Holmstrup Reference Holmstrup2018), tardigrades (Somme 1996), nematodes (Wharton & Ferns Reference Wharton and Ferns1995, McGill et al. Reference McGill, Shannon, Pisani, Felix, Ramløv and Dix2015), rotifers (Rebecchi et al. Reference Rebecchi, Boschetti and Nelson2020) and the sub-Antarctic midge Belgica antarctica (Benoit et al. Reference Benoit, Lopez-Martinez, Elnitsky, Lee and Denlinger2009). Certain groups can reduce their metabolism to almost zero, including tardigrades (Altiero et al. Reference Altiero, Giovannini, Guidetti and Rebecchi2015), and some species of nematodes secrete anti-freezing proteins (Adhikari et al. Reference Adhikari, Wall and Adams2009). Such adaptations are thought to have aided their persistence in refugia during glacial maxima.
Phylogeographic analyses
Phylogeography combines biogeographical information with phylogenetic analyses to assess patterns of speciation and colonization (Avise Reference Avise2000). The approach has shown how biotic responses to climatic and ecological conditions are constrained by geological context (Graham & Fine Reference Graham and Fine2008, Smith et al. Reference Smith, McCormack, Cuervo, Hickerson, Aleixo and Cadena2014), such as the strong relationship between refugia and diversity. High-resolution distributional data for soil invertebrates supported the demarcations of Antarctic bioregions (Terauds et al. Reference Terauds, Chown, Morgan, Peat, Watts and Keys2012). These partitions were informed by detailed biogeographical studies based on the morphological traits of soil invertebrates (Gressitt Reference Gressitt, Mieghern and Oye1965, Wallwork Reference Wallwork1973, Adams et al. Reference Adams, Wall, Virginia, Broos and Knox2014) and comprehensive floral records (Peat et al. Reference Peat, Clarke and Convey2007). Among the key divisions is the ‘Gressitt Line', a confirmed biotic frontier separating the Antarctic Peninsula (also known as Graham Land) and Continental Antarctica (Fig. 1; Pugh & Convey Reference Pugh and Convey2008). This division is accompanied by substantial genetic divergence and limited overlap in species, suggesting the presence of multiple refugia on either side of the division (Chown & Convey Reference Chown and Convey2007). Rigorous statistical pipelines using intra- and inter-specific differences can help us to assess theories of persistence, divergence and migration (Arbogast & Kenagy Reference Arbogast and Kenagy2001). With genealogies subject to repeated colonization events at the local scale (< 1 Ma), molecular phylogenetic assessment is the best approach to resolve evolutionary histories.
Molecular taxonomy
DNA sequencing allows the measurement of genetic divergence within and among species, thereby improving phylogenetic reconstructions (Thomson et al. Reference Thomson, Pyle, Ahyong, Alonso-Zarazaga, Ammirati and Araya2018). DNA barcoding is now commonly applied to identify putative species of soil fauna (Hebert et al. Reference Hebert, Cywinska, Ball and Dewaard2003). Routinely used markers are based on mitochondrial DNA (mtDNA) and nuclear DNA. Slower-evolving nuclear markers can show ancient lineages, although lower taxonomic orders may be less well resolved. However, the ability to resolve lineages is dependent upon the study taxa and genetic markers. The mtDNA cytochrome oxidase subunit I (COI) gene is a reliable identifier due to universal amplification and sufficient genetic variation between species but limited within-species differences (Hebert et al. Reference Hebert, Cywinska, Ball and Dewaard2003). Haplotype networks of COI have been used to resolve lineages of ancient populations of Collembola (Greenslade et al. Reference Greenslade, Stevens, Torricelli and D'Haese2011) and Lepidoptera (Hebert et al. Reference Hebert, Cywinska, Ball and Dewaard2003).
Delineation of operational taxonomic units (OTUs) is based on differences in COI nucleotide sequence, with values < 1% generally considered to be indicative of the same species (Hebert et al. Reference Hebert, Cywinska, Ball and Dewaard2003, Lim et al. Reference Lim, Balke and Meier2012). An interchangeable term is the haplotype, originally used to define lineages, whereby 2–3% is the minimum difference defining a distinct species, distances > 5% indicate divergent species/genera and those > 10% indicate highly divergent lineages (Stevens et al. Reference Stevens, Frati, McGaughran, Spinsanti and Hogg2007, Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019). Most studies use 3% as a threshold to define invertebrate species, as has been used in rotifers (Fontaneto et al. Reference Fontaneto, Kaya, Herniou and Barraclough2009) and nematodes (Kumari et al. 2010). Comparing results across taxa with broad ranges (e.g. the springtail Cryptopygus antarcticus) can further test the applicability of ‘rule-of-thumb’ thresholds across regions. Potential effects of selecting alternative thresholds for species delineation would be shifted diversity metrics or dating of species histories or dispersal events, but doing so will have minimal influence on the interpretation of phylogeographic analyses. Similarly, cytochrome oxidase-subunit II (COII) is an alternative in species where COI is less informative (e.g. cnidarians) due to minimal genetic variation in the marker, and it has been sequenced in Antarctic springtails (Stevens et al. Reference Stevens, Frati, McGaughran, Spinsanti and Hogg2007, McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011).
An increasing number of studies use nuclear markers to support species classification, identification of ancient speciation events (Reitzel et al. 2013) and isolation by distance across the landscape (Teske et al. Reference Teske, Golla, Sandoval-Castillo, Emami-Khoyi, Van Der Lingen and Von Der Heyden2018). Such studies commonly target ribosomal DNA (rDNA) genes that encode the small 40S ribosomal subunit including ETS, 18S, ITS1, 5.8S, ITS2 and 28S tandem repeat marker genes (Hwang & Kim Reference Hwang and Kim1999, Adams et al. Reference Adams, Wall, Gozel, Dillman, Chaston and Hogg2007, Evans & Paulay Reference Evans and Paulay2012). The thresholds for species delineation using nuclear 28S markers histone-3 (H3) and D2-D3 extension sequences have been shown to be as low as 0.1–0.5% in comparative studies (Klimov et al. 2019). The 18S rRNA genes have high levels of genetic drift and are frequently used to resolve taxonomic uncertainties at the species and genus level (Guidetti et al. Reference Guidetti, Rebecchi, Cesari and Mcinnes2014), as demonstrated in nematodes (Boström et al. Reference Boström, Holovachov and Nadler2011), tardigrades (Guil et al. Reference Guil, Jørgensen and Kristensen2019) and springtails (Zhang et al. Reference Zhang, Chen, Mateos, Scheu and Schaefer2019). The 28S rRNA markers have also yielded insights into the phylogenies of the marine Styraconyxidae tardigrades using a combination of 28S rRNA and COI markers (Fujimoto et al. Reference Fujimoto, Suzuki, Ito, Tamura and TSUJIMOTO2020), while COI and internal transcribed spacer 1 (ITS1) were sequenced to determine genetic diversity and to test theories of dispersal between Victoria Land (VL) and other Antarctic regions of Acutuncus antarcticus (Cesari et al. Reference Cesari, Mcinnes, Bertolani, Rebecchi and Guidetti2016). Additionally, 18S rRNA and ITS1-2 markers have revealed deep lineages in Scottnema lindsayae nematode populations across defined geographical areas (Adams et al. Reference Adams, Wall, Gozel, Dillman, Chaston and Hogg2007). Other single-copy nuclear genes, such as the H3 gene that structures the nucleosome, and commonly associated with epigenetics, have been used to assess levels of shared ancestry and phylogeographic dispersal among Antarctic mites (Mortimer et al. Reference Mortimer, Van Vuuren, Lee, Marshall, Convey and Chown2011), while the well-conserved Wnt signalling pathway genes have been targeted in tardigrades (Hodgson et al. Reference Hodgson, Convey, Verleyen, Vyverman, McInnes and Sands2010), and the wingless gene (Wg) has been used to identify intergeneric and interspecific mite taxonomies (Czechowski et al. Reference Czechowski, Sands, Adams, D'Haese, Gibson, Mcinnes and Stevens2012).
Molecular clocks
Molecular clocks are an essential part of estimating when divergence events occurred. The homogeneous substitution rate across the mitochondrial genome (mitogenome) simplifies their use in dating (Czechowski et al. Reference Czechowski, Clarke, Cooper and Stevens2017a,b). Secondary calibration that accounts for the uncertainty of phylogenetic-based calibration applies corrections to earlier calibrations (Kodandaramaiah Reference Kodandaramaiah2011, Schenk Reference Schenk2016). This has been shown to improve the accuracy of molecular clocks (Hipsley & Müller Reference Hipsley and Müller2014), such as that used in dating marine invertebrates (Loeza-Quintana et al. Reference Loeza-Quintana, Carr, Khan, Bhatt, Lyon, Hebert and Adamowicz2019). In the absence of verified ages for indigenous Antarctic taxa, studies commonly use molecular substitution rates derived from non-Antarctic insect phylogenies, with a consensus formed for an evolutionary rate (R) for arthropods of R = 1.5–2.3% Ma−1 (Stevens & Hogg Reference Stevens and Hogg2006, Brewer et al. Reference Brewer, Spruill, Rao and Bond2012, Beet et al. Reference Beet, Hogg, Collins, Cowan, Wall and Adams2016). Basing arthropod evolution on insect-based calibrations causes overestimation of dating due to the potentially faster generation times of insects (Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019).
More recently, geological events have been used to calibrate molecular clocks. These calibrations have benefitted from computational models being used to date warmer periods and ice-sheet collapses for invertebrate analyses (Strugnell et al. Reference Strugnell, Pedro and Wilson2018, Collins et al. Reference Collins, Hogg, Convey, Sancho, Cowan and Berry Lyons2020). This has led to a revised rate of R = 3.54% Ma−1 being used for Antarctic springtails (Papadopoulou et al. Reference Papadopoulou, Anastasiou and Vogler2010). The differences in R between non-Antarctic and Antarctic arthropods are considered to be a result of variation in coalescence times and post-separation gene flow (Collins et al. Reference Collins, Hogg, Convey, Sancho, Cowan and Berry Lyons2020). Additional factors that can improve estimations of divergence times include knowledge of generation time, metabolism and mutation rates and population size. The parthenogenetic, or asexual, nature of many oribatid mites also allows molecular clocks to be used without the complication of sexual recombination (Maraun et al. Reference Maraun, Heethoff, Scheu, Norton, Weigmann and Thomas2003). Yet these can yield misleading ages if rates are compared with sexually reproducing taxa. Bayesian relaxed clocks can incorporate variable estimates when setting priors, yet selection bias between competing models and variable mutation rates and generation times in natural systems mean dates are still only best estimates and can only be used as guides for relative divergence times (Guidetti et al. Reference Guidetti, McInnes, Cesari, Rebecchi and Rota-Stabelli2017). Additionally, secondary calibrations of studies relying on single calibration points might compound the unreliability of using geological events in the absence of fossils (Forest Reference Forest2009).
Phylogeographic studies of Antarctic soil fauna
Antarctica is an ideal location to study the biogeographical history of soil fauna due to the high proportion of endemic species and relatively limited dispersal, both within regions and from further afield. Here, a synthesis of the evidence across all phylogeographical studies is presented to form a clearer picture of general patterns of Antarctic soil faunal distribution and evolutionary patterns based on the current literature. Most studies focus on individual taxa and regions, but comparative studies that combine analyses of taxa and/or regions can more rigorously test alternative hypothesis while providing greater explanatory power. Unless specifically stated when referring to studies, all records refer to the alpha-taxonomic nomenclature as named in the cited works.
Collembola
Springtails, of the arthropod subclass Collembola, were the first Antarctic invertebrates to be described (Carpenter Reference Carpenter and Lankester1902). Since their discovery, 17 continental and 25 maritime species representing 4 families having been recorded (McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011), with almost two-thirds of all genera being endemic (Stevens & Hogg Reference Stevens and Hogg2003, Reference Stevens and Hogg2006, Pugh & Convey Reference Pugh and Convey2008, Torricelli et al. Reference Torricelli, Carapelli, Convey, Nardi, Boore and Frati2010b). Phylogeographical work has mostly focused on springtails of continental VL (71.0–78.5°S) in eastern Antarctica and on the peninsula. Three species are present in both continental and maritime regions: Cryptopygus antarcticus, Cryptopygus terranovus Wise, 1967, and Kaylathalia klovstadi Carpenter, Reference Carpenter and Lankester1902. What was once considered the sole circumpolar species, Friesea grisea Schaffer, 1891 (initially named Friesea antarctica Willem, 1901), has been taxonomically reassessed, resulting in the recognition of multiple species with smaller ranges, including Friesea propria Greenslade and Fanciulli, 2020 and Friesea gretae Greenslade and Fanciulli, 2020 (Carapelli et al. Reference Carapelli, Greenslade, Nardi, Leo, Convey, Frati and Fanciulli2020b, Stevens et al. Reference Stevens, Greenslade and D'Haese2021). F. grisea is now considered to be restricted to sub-Antarctic South Georgia alongside Friesea fantaba Greenslade, Reference Greenslade2018. An additional three species are found in continental southern VL (sVL): Antarcticinella monoculata Salmon, 1965, Cryptopygus nivicolus Salmon, 1965, and Gomphiocephalus hodgsoni Carpenter, 1908 (Greenslade Reference Greenslade2018, Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019). Taxonomic and phylogeographical studies have described local distributions and provided some insights into the ancient origins and restricted gene flow between populations arising from refugial survivors on the continent and other Antarctic regions.
Origins and refugia
Phylogeographical studies have improved theories of springtail origins, with a consensus being established of most taxa evolving from ancestors arriving on the continent ~20 Ma, prior to the formation of the ACC (Fig. 3; Stevens et al. Reference Stevens, Greenslade, Hogg and Sunnucks2006a, Stevens & D'Haese Reference Stevens and D'Haese2014). Several factors have promoted speciation, with several endemic species identified using molecular data, indicating more recent evolution (Table I). Intermittent dispersal events from surrounding sub-Antarctic landmasses and inland refugia may have contributed to the allopatric speciation of populations separated by glaciers and other dispersal barriers (Convey & Stevens Reference Convey and Stevens2007, McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011). Springtails show evidence of complex evolutionary histories, with certain species linked to ancient arrivals and others to more recent colonization events (Table II). The latter point to a series of post-glacial recolonization events followed by vicariant speciation. Significant divergence and a lack of shared haplotypes between continental and maritime springtail species suggest substantial dispersal barriers and long-term persistence in distinct refugia from which source populations remained separated following dispersal events (Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019, Reference Collins, Hogg, Convey, Sancho, Cowan and Berry Lyons2020). Most studies found glaciers to be major dispersal barriers, restricting gene flow (Stevens et al. Reference Stevens, Greenslade, Hogg and Sunnucks2006a, Bennett et al. Reference Bennett, Hogg, Adams and Hebert2016, Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019). This has led to the assumption of there being multiple refugia in glacial valleys throughout continental VL as the source for distinct haplotypes of C. terranovus (Carapelli et al. Reference Carapelli, Leo and Frati2017a) and K. klovstadi populations (Fig. 4a; Frati et al. Reference Frati, Spinsanti and Dallai2001).
Figure 3. Graphical timeline of invertebrate groups and earliest indications of endemic Antarctic lineage. Ages are based on mean estimated origins from molecular dating studies in Continental Antarctica alongside main regional geological events over a logarithmic timeline; 1 Ga = 1000 Ma (adapted from Convey Reference Convey2010). ACC = Antarctic Circumpolar Current; Ka = thousand years ago; LGM = Last Glacial Maximum; Ma = million years ago.
Table I. Currently known species richness of the main invertebrate groups in continental (C), maritime (M) and sub-Antarctic (S) regions, alongside the sequenced genes for all species found within each region and estimated date of origin from cited references.
Ka = thousand years ago; LGM = Last Glacial Maximum; Ma = million years ago.
Table II. Examples of the main Antarctic faunal types and species that have phylogenetic evidence supporting either their ancient origins or more recent dispersal in continental and maritime regions.
LGM = Last Glacial Maximum.
Figure 4. a. Map of Victoria Land (VL) with major glacial features and compiled results from phylogeographical studies. Springtail geographical ranges are indicated by coloured lines on the left panel from McGaughran et al. (Reference McGaughran, Hogg and Stevens2008), with theorized dispersal routes to Ross Island from Stevens & Hogg (Reference Stevens and Hogg2003) and Collins et al. (Reference Collins, Hogg, Convey, Barnes and McDonald2019, Reference Collins, Hogg, Convey, Sancho, Cowan and Berry Lyons2020). Dashed lines demarcate biotic boundaries used to define population groups, with symbols representing genetically distinct populations of springtails (yellow triangles), mites (red circles), nematodes (green circles) and rotifers and tardigrades (purple squares; sources: Barrett et al. Reference Barrett, Virginia, Wall, Cary, Adams, Hacker and Aislabie2006, Torricelli et al. Reference Torricelli, Frati, Convey, Telford and Carapelli2010a, McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011, Convey et al. Reference Convey, Chown, Clarke, Barnes, Bokhorst and Cummings2014, Brunetti et al. Reference Brunetti, Siepel, Fanciulli, Nardi, Convey and Carapelli2021b). b. Map of the Antarctic Peninsula (Graham Land), with theorized dispersal routes between springtail populations indicated by red arrows from McGaughran et al. (Reference McGaughran, Stevens and Holland2010a). Symbols represent genetically distinct populations of midges (orange circles) and potential refugial locations (empty squares; sources: Torricelli et al. Reference Torricelli, Frati, Convey, Telford and Carapelli2010a, Allegrucci et al. Reference Allegrucci, Carchini, CONVEY and Sbordoni2012, Convey et al. Reference Convey, Chown, Clarke, Barnes, Bokhorst and Cummings2014, Velasco-Castrillón et al. Reference Velasco-Castrillón, Page, Gibson and Stevens2014b, Carapelli et al. Reference Carapelli, Convey, Frati, Spinsanti and Fanciulli2017b).
Several studies support the refugial theory and the potential for multiple source populations (Marshall & Coetzee Reference Marshall and Coetzee2000, Fanciulli et al. Reference Fanciulli, Summa, Dallai and Frati2001, Frati et al. Reference Frati, Spinsanti and Dallai2001, Stevens & Hogg Reference Stevens and Hogg2006, McGaughran et al. Reference McGaughran, Hogg and Stevens2008). Evidence from the Friesea genus shows potential colonization by a common ancestor > 20 Ma (Miocene/Oligocene), with subsequent local speciation occurring and no haplotype sharing between the Antarctic Peninsula and VL regions (Torricelli et al. Reference Torricelli, Carapelli, Convey, Nardi, Boore and Frati2010b, Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019), nor between the Antarctic Peninsula and South Shetland Islands (Torricelli et al. Reference Torricelli, Frati, Convey, Telford and Carapelli2010a).
The northern VL (nVL) species K. klovstadi (formerly Isotoma klovstadi and of the Desoria genus) show divergences between subspecies that are geographically close to each other, further supporting multi-refugial sources (Stevens et al. Reference Stevens, Fjellberg, Greenslade, Hogg and Sunnucks2006b, Reference Stevens, Frati, McGaughran, Spinsanti and Hogg2007, Stevens & D'Haese Reference Stevens and D'Haese2016). The identification of different dominant haplotypes of K. klovstadi between the peninsular Adelaide, Lagoon and Killingbeck islands led to theories of separate lineages, with multiple refugial populations undergoing rapid evolution throughout the Pleistocene (Fig. 4b; Hawes et al. Reference Hawes, Worland, Bale and Convey2008). These patterns of distribution following refugial dispersal have also been observed on the Antarctic continent (Carapelli et al. Reference Carapelli, Cucini, Fanciulli, Frati, Convey and Nardi2020a). Another study that supports the idea of multiple refugia maintaining isolated populations found lower-than-expected genetic distances between G. hodgsoni populations on the peninsula, indicating a scenario whereby dispersal from a singular refugial source was followed by minimal genetic admixing (McGaughran et al. Reference McGaughran, Torricelli, Carapelli, Frati, Stevens, Convey and Hogg2010c).
Dispersal effects on broad-scale and regional distribution
Springtails are highly motile at short ranges and more infrequently disperse longer distances via wind or water-borne flotation (Hawes et al. Reference Hawes, Worland, Bale and Convey2008, McGaughran et al. Reference McGaughran, Stevens and Holland2010a). There is evidence of high rates of divergence among haplotypes and patchy distributions of Friesea spp., C. antarcticus subspecies and C. cisantarcticus populations in maritime regions and continental VL (Table III; McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011).
Table III. Summary of mean levels of COI and COII sequence divergence and number of haplotypes in springtail species and regions as reported in cited references.
Note: The taxonomy of F. grisea has since been revised, and it is now known to represent four unique species, namely F. grisea, F. antarctica, F. gretae and F. propria.
AP = Antarctic Peninsula; N = northern; S = southern.
The nVL C. cisantarcticus was studied alongside the sVL springtail G. hodgsoni, with lower genetic diversity between C. cisantarcticus haplotypes signalling multiple dispersals from elsewhere in the continent during the Pleistocene (McGaughran et al. Reference McGaughran, Hogg and Stevens2008). These data support an earlier study that also found minimal divergence within C. cisantarcticus populations (Hawes et al. Reference Hawes, Torricelli and Stevens2010), suggesting a Pliocene divergence event ~5 Ma, with distributional patterns indicative of recent gene flow from local refugia to the continental foothills.
Evidence of refugia as sources of ancient dispersal and broad-scale distribution has also been found regarding more recent dispersal events that have contributed to complex regional distribution patterns. Accordingly, Friesea spp. populations were suspected of more recent dispersal than C. terranovus or G. hodgsoni populations from unidentified regional refugia. These aligned with the shorter intervals between glacial cycles and barriers to dispersal preceding the LGM (Table III; Warren et al. Reference Warren, Cardillo, Rosauer and Bolnick2014, Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019). Furthermore, Collins et al. (Reference Collins, Hogg, Convey, Barnes and McDonald2019) found much higher divergences between C. cisantarcticus populations than between K. klovstadi populations across a similar geographical range: that of an individual glacier. Yet, lower divergences between populations in an adjacent glacier were the result of greater dispersal abilities of C. cisantarcticus influencing distribution patterns (Stevens et al. Reference Stevens, Fjellberg, Greenslade, Hogg and Sunnucks2006b, McGaughran et al. Reference McGaughran, Stevens and Holland2010a; Carapelli et al. Reference Carapelli, Leo and Frati2017a).
A study that combined G. hodgsoni with two species from sVL (C. nivicolus and A. monoculata) estimated a speciation event ~4 Ma, followed by glacial isolation that promoted speciation in G. hodgsoni and C. nivicolus over A. monoculata populations. A period of isolation between 3 and 4 Ma matched the collapse and reformation of the West Antarctic Ice Sheet (Beet et al. Reference Beet, Hogg, Collins, Cowan, Wall and Adams2016). The link between populations and access to liquid water was given as a cause for highly divergent G. hodgsoni populations (Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019).
Evidence from phylogeographical studies of Antarctic springtails reveals that at the broad scale interactions with climate and geography have created multilayered patterns of distribution following waves of speciation and extinction during the Pleistocene (~2.58 Ma–12 Ka), with some events separated by 100 Ka (Huybers Reference Huybers2006). These findings show that springtails have ancient lineages and underwent recent inter-regional dispersal (Table II), with glaciers restricting gene flow between populations and communities. It is speculated that more widespread sampling will show pockets of unaccounted speciation, confirming refugial locations in the peninsula and identifying further pan-Antarctic species.
Acari
The Acari, or mites, are the most diverse faunal group in terrestrial Antarctica (Pugh Reference Pugh1993). Current tallies number 105 species consisting of 5 continental, 22 maritime and 78 sub-Antarctic species, of which ~70 are endemic (Convey Reference Convey2011, McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011). The biogeography of several mite species has been surveyed on the sub-Antarctic islands (Mortimer et al. Reference Mortimer, Van Vuuren, Lee, Marshall, Convey and Chown2011) and Maritime Antarctica, with limited evidence of biogeographical patterns on the continent; despite evidence of structured distributions in VL (Collins et al. 2023), most distributions remain unverified using molecular approaches.
Origins and refugia
First described from the Belgica expedition of 1897–1899 (de Man Reference DE MAN1904), continental mites have some of the earliest links to a pre-Gondwanan lineage (Fig. 3). Several species appear to have ancient origins, including members of the oribatid mite genus Maudheimia Dalenius and Wilson, 1958 (> 100 Ma; Marshall & Coetzee Reference Marshall and Coetzee2000) and the prostigmatid mite genus Stereotydeus Berlese, 1901 mites (> 10 Ma; Stevens & Hogg Reference Stevens and Hogg2006). While some mites have an ancient origin, it is difficult to ascribe all Antarctic taxa as having ancient lineages (Table II). Molecular analyses have shown that vicariant speciation was prevalent during interglacial periods in mites (Stevens & Hogg Reference Stevens and Hogg2006), similar to observed patterns in springtails (McGaughran et al. Reference McGaughran, Hogg and Stevens2008). There is evidence of local refugia with oribatid and prostigmatid mites persisting during glacial maxima, and most Antarctic mites appear to have dispersed from glacial refugia and coastal habitats (Marshall & Coetzee Reference Marshall and Coetzee2000).
Dispersal effects on broad-scale and regional distribution
Despite their ability for long-distance dispersal, the little overlap between continental and maritime populations demonstrates strong geographical barriers limiting dispersal among geographical regions (Convey et al. Reference Convey, Chown, Clarke, Barnes, Bokhorst and Cummings2014). However, there is evidence of some dispersal within regions. For example, a study of eight members of the genus Halozetes Berlese, 1916 in Maritime Antarctica and the sub-Antarctica islands found frequent dispersal events between the sub-Antarctic islands among H. belgicae and populations of the mite genus Alaskozetes Hammer, 1955 between 6 and 10 Ma, as well as a rare case of wind- or water-borne dispersal from northern peninsular refugia to surrounding islands (Table I; Mortimer et al. Reference Mortimer, Van Vuuren, Lee, Marshall, Convey and Chown2011).
Restrictions to dispersal and mixing of populations, evident from a lack of shared haplotypes and gene flow, may also indicate recent colonization of the sub-Antarctic islands and continent (Mortimer et al. Reference Mortimer, Van Vuuren, Lee, Marshall, Convey and Chown2011, Convey et al. Reference Convey, Chown, Clarke, Barnes, Bokhorst and Cummings2014). Limited ranges and high endemism have been shown in peninsular populations of H. belgicae and Alaskozetes antarcticus Michael, 1903, with further evidence of multiple refugial sources (Table II; Van Vuuren et al. Reference Van Vuuren, Lee, Convey and Chown2018). Additionally, contemporary distribution patterns conform with the limited short-range dispersal ability of mites, linked to their low desiccation tolerance (McGaughran et al. Reference McGaughran, Stevens and Holland2010a). Beyond this, molecular studies on the short-range dispersal of mites are limited.
Despite thorough biogeographical investigation (Block & Starý Reference Block and Starý1996, Marshall & Coetzee Reference Marshall and Coetzee2000, Collins et al. Reference Collins, Young, Convey, Chown, Cary and Adams2023), knowledge on the phylogeography of Antarctic mites is limited. However, studies have revealed restricted distributions of several mite species (Van Vuuren et al. Reference Van Vuuren, Lee, Convey and Chown2018), with diverse prostigmatid communities in inland oases (Lawley et al. Reference Lawley, Ripley, Bridge and Convey2004, Brunetti et al. Reference Brunetti, Siepel, Fanciulli, Nardi, Convey and Carapelli2021b). Phylogenetic support for their ancient lineages, combined with evidence of recent evolution linked to refugial dispersal, can be clarified through targeted sampling. This would overcome the data deficiency for these important decomposers and support arguments for their use of refugia and long-range dispersal as explanations of their diverse contemporary distribution.
Nematoda
The first terrestrial nematode to be described from Antarctica was Plectus antarcticus (de Man Reference DE MAN1904), and there are now 68 recognized species, including 23 continental and 33 maritime species, with most genera endemic to Antarctica and some shared species across regions (Maslen & Convey Reference Maslen and Convey2006, Nielsen et al. Reference Nielsen, Wall, Adams and Virginia2011a, Kagoshima et al. Reference Kagoshima, Maslen, Kito, Imura, Niki and Convey2019). However, the recorded diversity of nematodes is considered a gross underestimate (Nielsen et al. Reference Nielsen, Wall, Li, Toro, Adams and Virginia2011b, Velasco-Castrillón et al. Reference Velasco-Castrillón, Gibson and Stevens2014a, Nielsen & King Reference Nielsen and King2015).
Origins and refugia
Nematodes were well established throughout the Gondwanan continent, and molecular data confirm the ancient origins (> 32 Ma) of most, if not all, indigenous Antarctic taxa (Fig. 3; Maslen & Convey Reference Maslen and Convey2006, Adams et al. Reference Adams, Wall, Gozel, Dillman, Chaston and Hogg2007). High levels of cryptic speciation and low levels of divergence between most nematode genera (< 5%) indicate recent speciation (Adams et al. Reference Adams, Wall, Virginia, Broos and Knox2014). This is evidenced by a combination of ancient species, such as Scottnema lindsayae (Maslen & Convey Reference Maslen and Convey2006), and those with more recent divergence, including Panagrolaimus davidi Timm, 1971 (Table II; Lewis et al. Reference Lewis, Dyal, Hilburn, Weitz, Liau, Lamunyon and Denver2009). Antarctica's cyclical glaciation split some nematode species across maritime and continental regions, suggesting separate refugial origins (Andrássy Reference Andrássy1998). Additionally, high nematode endemism on Alexander Island (> 40%) and other sites along the peninsula indicate probable long-term refugial isolation and survival in these areas (Maslen & Convey Reference Maslen and Convey2006).
Dispersal effects on broad-scale and regional distribution
The phylogeographical patterns of nematodes indicate their ancient origins, refugial survival and widespread contemporary distribution. Molecular studies of nematodes indicate evolutionary histories as ancient as those of the arthropods, showing them to be equally dependent on refugia for their survival. High levels of cryptic speciation within endemic taxa warrant further investigation to determine their in situ diversity, speciation and evolutionary processes such as convergence or stasis (Struck et al. Reference Struck, Feder, Bendiksby, Birkeland, Cerca and Gusarov2018).
General patterns of nematode distribution are influenced at multiple scales. Minimal genetic variation in southern maritime island S. lindsayae populations, despite large distances between populations, could indicate a population bottleneck or gene flow with limited genetic drift of these highly adapted ancient taxa following isolation (Maslen & Convey Reference Maslen and Convey2006). Concerted evolution of ITS genes may remove intraspecific variation (Álvarez & Wendel Reference Álvarez and Wendel2003), unlike mtDNA markers (e.g. COI); however, the variation among species is also dependent upon the age of the lineages and differs between taxa (Evans & Paulay Reference Evans and Paulay2012).
Nematode COI sequences from the Larsemann and Vestfold hills in continental eastern Antarctica showed limited divergence among populations of Plectus murrayi Yeates, 1970 (< 0.5%), suggesting a high degree of connectivity. In contrast, the higher divergence rates among Plectus frigophilus Kiryanova, 1958 populations (8.4%) suggest cryptic speciation and taxonomic division. The contrast between P. murrayi and P. frigophilus indicates restricted gene flow in the latter species, probably because it requires more persistent bodies of water for dispersal success (Table I; Velasco-Castrillón et al. Reference Velasco-Castrillón, Page, Gibson and Stevens2014b,c).
A more detailed understanding of these distributional ranges would improve our dating of nematode phylogenies. Constraints to robust phylogeographical modelling may be due to suspected differences in substitution rates from differences in reproductive mode and other biotic factors between species. Further investigation may reveal more widespread continental nematode species and help explain the high levels of endemism despite their ability for long-range dispersal.
Rotifera
Antarctic rotifers were among the earliest reports of terrestrial fauna from Scott's 1901–1904 Discovery expedition, for which an ancient origin was initially hypothesized (Murray Reference Murray1910). Rotifers are semi-aquatic and generally parthenogenetic organisms capable of wind- and water-borne dispersal and anhydrobiosis. There are presently 94 recorded rotifer species, of which 66 are continental, with the remainder distributed throughout the maritime and sub-Antarctic islands (Velasco-Castrillón & Stevens Reference Velasco-Castrillón and Stevens2014); however, rotifer richness and therefore endemicity are probably underestimated. Most rotifers have links to corresponding species from other Southern Hemisphere continents, while only five species are endemic to the continent (Velasco-Castrillón et al. Reference Velasco-Castrillón, Page, Gibson and Stevens2014b), and one is shared across Maritime and Continental Antarctica (Table I; Segers Reference Segers2008, Iakovenko et al. Reference Iakovenko, Smykla, Convey, Kašparová, Kozeretska and Trokhymets2015).
Origins and refugia
The relatively limited genetic variation between Antarctic and non-Antarctic species points to a far more recent arrival of rotifers than other taxa (Fig. 3; Iakovenko et al. Reference Iakovenko, Smykla, Convey, Kašparová, Kozeretska and Trokhymets2015, Cakil et al. Reference Cakil, Garlasché, Iakovenko, Di Cesare, Eckert and Guidetti2021). A plausible scenario for this is that arrivals commenced ~130 Ka based on sedimentary evidence of Notholca Gosse, 1886 from the Larsemann Hills of East Antarctica (Cromer et al. Reference Cromer, Gibson, Swadling and Hodgson2006). This could be a result of their inability to survive previous ice ages due to limited cold-tolerant traits, alongside their ability for long-distance wind dispersal and the presence of multiple refugial lakes (Shain et al. Reference Shain, Halldórsdóttir, Pálsson, Aðalgeirsdóttir, Gunnarsson and Jónsson2016). The continental ranges of some Adineta Hudson and Gosse, 1886 bdelloid species extend up to 2000 km (Velasco-Castrillón et al. Reference Velasco-Castrillón, Schultz, Colombo, Gibson, Davies, Austin and Stevens2014c) and remain to be assessed using phylogenetic records. Antarctic bdelloid rotifers show strong patterns of increased genetic divergence with greater isolation than other non-Antarctic specimens, indicating greater periods of isolation and separation beyond what can be concluded from the molecular evidence alone (Cakil et al. Reference Cakil, Garlasché, Iakovenko, Di Cesare, Eckert and Guidetti2021).
Dispersal effects on broad-scale and regional distribution
A thorough study of COI sequences from 514 rotifer specimens collected across all Antarctic regions revealed a total of 92 species, with 63 found throughout continental and maritime regions (Velasco-Castrillón et al. Reference Velasco-Castrillón, Gibson and Stevens2014a), while 7 continental species were distributed across 13 lakes (Velasco-Castrillón et al. Reference Velasco-Castrillón, Schultz, Colombo, Gibson, Davies, Austin and Stevens2014c). The presence of three pan-Antarctic rotifer species indicates prolonged isolation (Adineta grandis Murray, 1910, Philodina antarctica Murray, 1910 and Philodina gregaria Murray, 1910) but does not fully explain the high numbers of shared haplotypes with non-Antarctic regions (Pugh & Convey Reference Pugh and Convey2008). Rotifer studies of Signy Island and Tierra del Fuego in South America also indicate that rotifer diversity is highly underestimated. Sequences from 210 individuals from multiple Antarctic and non-Antarctic locations revealed 36 taxa with up to 3.6% between-species divergence for four Adineta species, while species divergence ranged from 0.5% to 10.3% between 55 populations (Fontaneto et al. Reference Fontaneto, Iakovenko, Eyres, Kaya, Wyman and Barraclough2011), clearly raising the issue of cryptic species. With a high level of cryptic speciation and undescribed species, the parthenogenetic nature of rotifers may complicate their evolutionary histories.
Regional dispersal of rotifers has been described as random and often co-occurring with tardigrades that share cold-adaptive traits (Zawierucha et al. Reference Zawierucha, Kolicka, Takeuchi and Kaczmarek2015). Furthermore, fossil evidence of rotifers present in lakes in the eastern continental Vestfold Hills does not allow us to distinguish between the refugial or dispersal histories (Swadling et al. Reference Swadling, Dartnall, Gibson, Saulnier-Talbot and Vincent2001). More sequence information is required to assess regional dispersal patterns in rotifers (Sohlenius & Boström Reference Sohlenius and Boström2005).
In summary, the association of rotifers with refugia may demonstrate limited dispersal ability and motility and may explain their distributions that might be linked to unknown refugia. Further analysis is required to reveal their evolutionary history and to verify the hypothesis of rapid post-LGM colonization and speciation. Targeted sampling to locate refugia in the eastern continental hills could also be used to assess their ability for long-range dispersal. Future genomic studies may reveal more information about these complex gene pools, potentially re-evaluating theories of a more ancient origin for rotifers.
Tardigrada
A total of 64 species of limno-terrestrial tardigrades, or water bears, have been recorded throughout Continental and Maritime Antarctica, with approximately half of all genera being endemic to the region (McInnes & Pugh Reference McInnes and Pugh2007). First described in Antarctica by Richters (Reference Richters1904), these ‘slow-steppers’ range from 0.05 to 1.20 mm in length and are renowned for their survival ability. They tolerate the extreme cold by utilizing cryptobiosis (Wright Reference Wright2001) and are capable of long-distance dispersal in a dormant state (Fontaneto Reference Fontaneto2019). Tardigrades are probably under-sampled throughout Antarctica, but the most broadly distributed continental species are Hypsibius antarcticu Richters, Reference Richters1904 and Milnesium tardigradum Doyère, 1840, with no discernible species overlap between the continent and the Maritime Antarctic (Table I; Cesari et al. Reference Cesari, Mcinnes, Bertolani, Rebecchi and Guidetti2016).
Origins and refugia
Phylogeographical analyses of the continental Echiniscus canadensis Murray, 1910 using nuclear markers revealed a Gondwanan arrival with a speciation event of the ancient lineage in the Eocene (32–48 Ma; Guidetti et al. Reference Guidetti, McInnes, Cesari, Rebecchi and Rota-Stabelli2017, Reference Guidetti, Massa, Bertolani, Rebecchi and Cesari2019), despite the inherent difficulties in dating tardigrade speciation (Table II). There is a lack of continental-wide surveys, but analysis of specimens from populations in Ellsworth Land in the west of the continent showed low-level genotypic endemism and divergence, implying an absence of local refugia, with subsequent Quaternary-period re-colonization by both endemic and cosmopolitan taxa (McInnes Reference McInnes2010). The probably ancient origin of tardigrades is supported by their well-known tolerance of harsh conditions.
Dispersal effects on broad-scale and regional distribution
Considering the relatively ancient origins of tardigrades, combined with their renowned ability for refugial survival, patterns of widespread distribution throughout Antarctic regions would be expected. A study including 343 Antarctic and non-Antarctic specimens identified 70 unique Antarctic haplotypes using 18S rRNA, of which 25 were shared between the sub-Antarctic islands and Antarctic Peninsula and four were shared between Marion and South Georgia islands. Minimal haplotype sharing between divergent populations suggested the presence of cryptic species, as genetic divergences are comparable to those found between the distinct species Milnesium antarcticum Tumanov, 2006 and M. tardigradum (Sands et al. Reference Sands, McInnes, Marley, Goodall-Copestake, Convey and Linse2008).
An analysis of 126 tardigrades from two nunataks ~30 km apart in the Sør Rondane Mountains in Queen Maud Land identified 89 COI, 67 18S rRNA and 22 Wg haplotypes within the Macrobiotidea and Hypsibiidea families (Czechowski et al. Reference Czechowski, Sands, Adams, D'Haese, Gibson, Mcinnes and Stevens2012). More recent genetic studies using COI and nuclear 18S markers of the Mesobiotus genus revealed deep geographical distinctions across continental populations, with potential species complexes (Short et al. Reference Short, Sands, McInnes, Pisani, Stevens and Convey2022).
Unexpectedly high levels of divergence indicate strong barriers to gene flow between communities based on 42 specimens collected from the base of the Antarctic Peninsula despite their geographical proximity (McInnes Reference McInnes2010). As tardigrade phylogenies include high levels of cryptic speciation, a long-term presence, especially in the mountainous nunataks, has been suggested (Altmaier et al. Reference Altmaier, Herpers, Delisle, Merchel and Ott2010). More detailed phylogeographical studies of Antarctic tardigrades may shed light on the balance between long-range dispersal and refugial survival.
Chironomidae
The only known Antarctic insects are wingless species of the globally diverse Chironomidae family of the Diptera order. Two midge species of the genus Belgica Jacobs, 1900 are present, with Belgica antarctica Jacobs, 1900 endemic to Maritime Antarctica and Belgica albipes Seguy, 1965 endemic to the Îles Crozet sub-Antarctic islands. Earlier studies have found evidence for post-LGM vicariance between sub-Antarctic and maritime regions (Allegrucci et al. Reference Allegrucci, Carchini, Todisco, Convey and Sbordoni2006). However, phylogenetic knowledge of the indigenous Diptera is limited. Eretmoptera murphyi Schaeffer 1914 that was palaeo-endemic to South Georgia was introduced to Signy Island in the 1960s (Allegrucci et al. Reference Allegrucci, Carchini, CONVEY and Sbordoni2012, Hughes et al. Reference Hughes, Pertierra and Walton2013).
Evidence for an ancient origin in the resident midges has been found from multiple sources. Divergence rates of 28S rRNA sequences found a single ancestral midge as the ancestor of the three known Antarctic species, estimated to have undergone a colonization event some 49 Ma (Allegrucci et al. Reference Allegrucci, Carchini, Todisco, Convey and Sbordoni2006). Additionally, four distinct B. antarctica and two B. albipes haplotypes are closely related to the E. murphyi lineages (Fig. 4b & Table I; Allegrucci et al. Reference Allegrucci, Carchini, CONVEY and Sbordoni2012). This supports an earlier study that found B. antarctica and E. murphyi distributions to result from vicariance with an ancient origin (Allegrucci et al. Reference Allegrucci, Carchini, Todisco, Convey and Sbordoni2006).
Representatives of the Belgica and Eretmoptera Kellogg, 1900 genera show minimal gene flow between peninsular and sub-Antarctic populations, probably due to their limited long-distance dispersal ability (Convey Reference Convey1992). The limited long-distance dispersal ability of the indigenous wingless chironomids reinforces vicariance as a principal driver of genetic diversity, with a wave of colonization moving south through the peninsula following the LGM (Pugh & Convey Reference Pugh and Convey2008). Getting a firm grasp on the genetic diversity of chironomids and other potential invasive insects should be central to conservation plans for vulnerable Antarctic ecosystems.
Synthesis
Origins and refugia
There is increasing evidence that most of the terrestrial invertebrate fauna of Maritime and Continental Antarctica have ancient lineages, although origins differ among taxa. Strong evidence of an ancient origin in mites stems from a lack of genetic admixture between Antarctic and non-Antarctic species dating as far back as 10–100 Ma (Marshall & Coetzee Reference Marshall and Coetzee2000, Stevens & Hogg Reference Stevens and Hogg2006). Yet this large range is indicative of the discrepancies found when estimating the origins of Antarctic taxa. The younger origins of rotifers represent an example of the difficulties of establishing an evolutionary timeline despite extensive comparison with non-Antarctic specimens (Cakil et al. Reference Cakil, Garlasché, Iakovenko, Di Cesare, Eckert and Guidetti2021). The parthenogenetic nature of rotifers may also mask ancient lineages but can be clarified by sequencing of sister lineages. In addition to parthenogenesis, other confounding factors that can lead to discrepancies in molecular clock calculations include exogenous gene uptake, horizontal gene transfer, rapid population fluctuations, dispersal and extinction (Brown Reference Brown2003, Ho & Phillips Reference Ho and Phillips2009). This is especially the case when dating rotifers. Further investigation of sample sets collected over larger spatial scales may suggest alternative theories on their age and arrival.
Certain parthenogenetic nematodes (e.g. Panagrolaimus davidi) are also difficult to accurately date, with estimates of origins ranging from 1.35 to 8.50 Ma depending on calculated generation times (Lewis et al. Reference Lewis, Dyal, Hilburn, Weitz, Liau, Lamunyon and Denver2009, Schiffer et al. Reference Schiffer, Danchin, Burnell, Creevey, Wong and Dix2019). Similar ages of Antarctic nematodes (~30 Ma), tardigrades (~40 Ma) and chironomids (~49 Ma) indicate parallel evolutionary timescales. By contrast, repeated recent colonization is evident from events for Antarctic rotifers preceding the LGM (~130 Ka). Parthenogenetic reproduction in some species of oribatid mite and springtail also complicates evolutionary analyses with assumptions of consistent rates of genetic drift and background mutation, although the dominant taxa reproduce sexually.
Sub-Antarctic and maritime mite and springtail populations have some degree of shared genealogy that points to repeated mixing of ancient survivors with motile dispersers during interglacial periods and rare trans-oceanic migrations. Founder populations from maritime islands subsequently underwent varying degrees of in situ speciation with localized extinction events (Rogers Reference Rogers2007). The lack of genetic divergence and motility of mite populations along the peninsula supports a refugial ancestry (Pugh & Convey Reference Pugh and Convey2008). Further evidence comes from localized diversity and reinforces the narrative of multiple dispersal events.
Refugial survival has a defining role in nematode distributions, with interglacial dispersal and fast adaptation to abiotic pressures being key to the establishment of new colonies. For example, nematodes can only actively move short distances and require passive long-distance dispersal to seek out suitable habitats. Mites and springtails are susceptible to desiccation, yet their capacity for passive long-distance dispersal depended on the minimal chance of arrival on vegetated ice-free land during periods of glacial maxima (Fig. 4b; Hawes et al. Reference Hawes, Worland, Bale and Convey2008).
Contributions of dispersal to broad- and regional-scale distribution patterns
Phylogeographical studies across all main faunal types have shown a range of species distributions (Table I). Strong biotic barriers and biogeographical divisions between the continent and peninsular populations form observable divergence patterns in springtails (McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011, Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019), mites (Pugh Reference Pugh1993), nematodes (Smith Reference Smith and Laws1984, Maslen & Convey Reference Maslen and Convey2006) and tardigrades (Cesari et al. Reference Cesari, Mcinnes, Bertolani, Rebecchi and Guidetti2016), although these are lacking for rotifers. At smaller scales, similar dispersal barriers were evident in multiple Antarctic regions within the continental Dry Valleys of VL (Fig. 4a; Stevens & Hogg Reference Stevens and Hogg2003, Barrett et al. Reference Barrett, Virginia, Wall, Cary, Adams, Hacker and Aislabie2006), the Antarctic Peninsula (Fig. 4b; Chown & Convey Reference Chown and Convey2007, McGaughran et al. Reference McGaughran, Torricelli, Carapelli, Frati, Stevens, Convey and Hogg2010c) and eastern Continental Antarctica (Fig. 4a; Velasco-Castrillón et al. Reference Velasco-Castrillón, Schultz, Colombo, Gibson, Davies, Austin and Stevens2014c). This distribution pattern aligns with the limited motility of nematodes (Adams et al. Reference Adams, Wall, Gozel, Dillman, Chaston and Hogg2007) and may also support a wind-borne theory of infrequent dispersal (Nkem et al. Reference Nkem, Wall, Virginia, Barrett, Broos, Porazinska and Adams2006, Ptatscheck et al. Reference Ptatscheck, Gansfort and Traunspurger2018). Localized distributions are even present in the circumpolar Cryptopygus springtails, giving phylogeographic support to an ancient origin for the genus (~24 Ma; Stevens et al. Reference Stevens, Greenslade, Hogg and Sunnucks2006a, McGaughran et al. Reference McGaughran, Hogg and Stevens2008, Reference McGaughran, Stevens, Hogg and Carapelli2011), with complex interactions with dispersal ability (McGaughran et al. Reference McGaughran, Stevens and Holland2010a). These contrast with the histories of G. hodgsoni and C. cisantarcticus that diverged > 1 Ma (Stevens & Hogg Reference Stevens and Hogg2006, Stevens et al. Reference Stevens, Greenslade, Hogg and Sunnucks2006a). This may also indicate the prominence of recolonization and dispersal events in shaping distributions. Long-distance dispersal among maritime and sub-Antarctic islands is also clear from mite (Mortimer et al. Reference Mortimer, Van Vuuren, Lee, Marshall, Convey and Chown2011) and springtail populations (Stevens et al. Reference Stevens, Greenslade, Hogg and Sunnucks2006a). These dispersal events have often been linked with refugial survival and long periods of inter-glacial isolation. This is apparent from molecular evidence for mites and springtails, with further investigation being required to confirm refugial origins for the non-arthropod nematodes, rotifers and tardigrades that have generally more limited dispersal abilities.
The pre-LGM dispersal events might be masked by more frequent post-LGM dispersal events, as evidenced in springtails (Hawes et al. Reference Hawes, Torricelli and Stevens2010, Carapelli et al. Reference Carapelli, Leo and Frati2017a) and potentially occurring in mites (Van Vuuren et al. Reference Van Vuuren, Lee, Convey and Chown2018). Recent speciation (< 20 Ka) in the prostigmatid Stereotydeus mollis Womersley and Strandtmann, 1963 and the sub-Antarctic oribatid H. fulvus mites supports a post-LGM theory of continental mite dispersal and speciation (Brunetti et al. Reference Brunetti, Siepel, Convey, Fanciulli, Nardi and Carapelli2021a). These findings align with an earlier, morphological-based study (Pugh & Convey Reference Pugh and Convey2008). Further comparisons of mites with Brachionus plicatilis Müller, 1786 showed marked similarities in divergences over similar ranges, whereby patterns of long-distance dispersal were constrained by local geography, with evidence of unsubstantiated refugia (Fontaneto et al. Reference Fontaneto, Kaya, Herniou and Barraclough2009).
A study of rotifers using molecular data from a defined transect within the Transantarctic Mountains found three species with limited cryptic speciation that were suggested to indicate limited starting diversity and restricted gene flow (Hodgson et al. Reference Hodgson, Convey, Verleyen, Vyverman, McInnes and Sands2010). Additionally, the widespread presence throughout the peninsula and sub-Antarctic islands of tardigrades is similar to those of rotifers and Southern Hemisphere nematodes (McInnes & Pugh Reference McInnes and Pugh1998, Reference McInnes and Pugh2007). Overcoming the data deficiency in Southern Hemisphere taxa may yet reveal more recent divergence events separating Antarctic taxa from species with shared ancestors on nearby landmasses, especially for the complex Rotifera. Sequences from regions with a Gondwanan history (e.g. South America, Sri Lanka, Australia and New Zealand) could be used to establish genetic distances and identify recent arrivals, as has been done for arachnids (Baker et al. Reference Baker, Sheridan, Derkarabetian, Pérez-González, Vélez and Giribet2020).
Local-scale distribution patterns
Fragmented habitats divided by glaciers and ice sheets are often associated with restricted gene flow and high levels of genetic differentiation, as observed in mites (Mortimer et al. Reference Mortimer, Van Vuuren, Lee, Marshall, Convey and Chown2011), springtails (Fanciulli et al. Reference Fanciulli, Summa, Dallai and Frati2001, Frati et al. Reference Frati, Spinsanti and Dallai2001, Stevens et al. Reference Stevens, Frati, McGaughran, Spinsanti and Hogg2007, McGaughran et al. Reference McGaughran, Stevens, Hogg and Carapelli2011) and chironomids (Allegrucci et al. Reference Allegrucci, Carchini, CONVEY and Sbordoni2012). The West Antarctic Ice Sheet was shown to be a strong barrier to dispersal. Marked increases in speciation followed its collapse 5 Ma created large disparities in diversity among populations found on either side of the West Antarctic Ice Sheet (Pollard & DeConto Reference Pollard and Deconto2009, Hawes et al. Reference Hawes, Torricelli and Stevens2010, McGaughran et al. Reference McGaughran, Convey, Stevens and Chown2010b, Bennett et al. Reference Bennett, Hogg, Adams and Hebert2016).
At local scales, biotic distributions are influenced by both local barriers and an organism's ability for passive wind- or water-borne long-term dispersal and active local motility. This is most apparent around glaciers and other dispersal barriers, where communities often have limited gene flow despite being geographically close to each other. These speciation events are balanced by extinctions that often follow waves of dispersal and colonization, ultimately contributing to the complex gene pools that are found in mite (Marshall & Coetzee Reference Marshall and Coetzee2000, Maraun et al. Reference Maraun, Heethoff, Scheu, Norton, Weigmann and Thomas2003) and springtail populations (McGaughran et al. Reference McGaughran, Hogg and Stevens2008, Reference McGaughran, Stevens, Hogg and Carapelli2011, Collins et al. Reference Collins, Hogg, Convey, Barnes and McDonald2019).
Nematodes, tardigrades and rotifers tend to be more locally endemic, with limited divergence and gene flow between populations, even within the ancient members of the nematode genus Scottnema Timm, 1971 (Adams et al. Reference Adams, Wall, Gozel, Dillman, Chaston and Hogg2007, Boström et al. Reference Boström, Holovachov and Nadler2011). Evidence of recent dispersal for mites and springtails contrasts with the less motile taxa, which tend to have a higher proportion of ancient lineages due to them being able to endure glaciation in situ. As such, they are associated with more cryptic speciation, as observed in persistent rotifer (Fontaneto et al. Reference Fontaneto, Iakovenko, Eyres, Kaya, Wyman and Barraclough2011) and tardigrade populations (Czechowski et al. Reference Czechowski, Sands, Adams, D'Haese, Gibson, Mcinnes and Stevens2012).
Future research priorities
Molecular approaches can further increase sampling depth to resolve biogeographical patterns in greater detail, pinpointing refugial locations (e.g. peninsular montane regions) and revealing population dynamics (Convey et al. Reference Convey, Chown, Clarke, Barnes, Bokhorst and Cummings2014). Spatial and temporal resolutions to within 1 km around single glacier or within a glacial cycle of 10 Ka (McGaughran et al. Reference McGaughran, Hogg and Stevens2008, Collins et al. Reference Collins, Hogg, Convey, Sancho, Cowan and Berry Lyons2020) can confirm repeated colonization events (Rogers Reference Rogers2007) and improve models of assemblage responses to ecosystem fragmentation (Struck et al. Reference Struck, Feder, Bendiksby, Birkeland, Cerca and Gusarov2018).
The similar morphological traits and life histories of the terrestrial arthropods, mites and springtails make them ideal candidates for interspecific comparison of functions between taxa and regions (Ross et al. Reference Ross, Berg, Salmon and Nielsen2022). Further developments in bioinformatics and statistical software can also advance phylogeographical analyses and hypothesis testing (Beheregaray Reference Beheregaray2008, Avise et al. Reference Avise, Bowen and Ayala2016). Meanwhile, comparisons with Gondwanan sister lineages can improve dating estimates. Studies have applied high-throughput sequencing, environmental DNA (eDNA) and genomic datasets to assess a range of soil biodiversity, including nematodes, rotifers and tardigrades from VL and maritime islands (Zawierucha et al. Reference Zawierucha, Porazinska, Ficetola, Ambrosini, Baccolo and Buda2021, Czechowski et al. Reference Czechowski, De Lange, Knapp, Terauds and Stevens2022) and from diverse oribatid mite assemblages in Australia (Ross et al. Reference Ross, Horn, MacDonald, Powell, Reynolds and Ryan2020). Divergences within C. cisantarcticus, which has low levels of cryptic speciation (relative to other Antarctic taxa) but higher mutation rates compared to other Cryptopygus spp., could help us to define OTU delimitation thresholds and levels of genetic drift. Detailed genomic datasets that are processed using automated learning algorithms have detailed evolutionary histories of the Plectus Laporte, 1840 nematodes (Xue et al. Reference Xue, Suvorov, Fujimoto, Dilman and Adams2020) and sub-Antarctic springtail subspecies C. cisantarcticus travei Deharveng, 1981 (Monsanto et al. Reference Monsanto, Jansen Van Vuuren, Jagatap, Jooste, Janion-Scheepers, Teske and Emami-Khoyi2019).
Single-nucleotide polymorphisms (SNPs), microsatellites and diversity array technology sequencing (DArTseq) are other approaches used to extract meaningful ecological information from genomic datasets (McGaughran et al. Reference McGaughran, Terauds, Convey and Fraser2019, Collins et al. Reference Collins, Hogg, Convey, Sancho, Cowan and Berry Lyons2020), while assemblage patterns have been inferred from metagenomics in mites, springtails and beetles (Arribas et al. Reference Arribas, Andújar, Hopkins, Shepherd and Vogler2016, Reference Arribas, Andújar, Moraza, Linard, Emerson and Vogler2020, Reference Arribas, Andújar, Salces-Castellano, Emerson and Vogler2021). It is hoped that combining molecular approaches with morphological taxonomy can highlight the importance of biodiversity to fragile ecosystems, enabling them to adapt to shifts in environmental conditions and to ensure their continued existence.
Author contributions
GMR and UNN conceptualized the study, with GMR collating the works and writing the first draft of the manuscript under the supervision of UNN. The final manuscript was reviewed and edited with input from PDR and JMC.
Acknowledgements
The authors thank Scott E. Bevins, Leah M. Carr, Peter Convey, Simon N. Larkman, David Randall, two reviewers and the editor for assisting in literature research, proofreading, imaging and constructive feedback on the manuscript.
Financial support
This research did not receive any specific funding from agencies in the public, commercial or non-profit sectors. GMR was supported by an Antarctic Science Foundation (AUS) PhD grant, a Western Sydney University PhD scholarship and a Research Training Program-funded placement at the Hawkesbury Institute for the Environment (HIE).
Competing interests
The authors declare none.
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