Origin and distribution of Mopsechiniscus
Biogeographical distribution and ecology of Mopsechiniscus speciesnext section
Reports of Mopsechiniscus species are largely confined to the Southern Hemisphere, with the most northern reference to be found for Costa Rica, and the majority of references from South America (Venezuela, Brazil, Argentina, and Chile), southern Australia, sub-Antarctic, and continental Antarctica (Fig. 1). In particular, four of the six described species are considered endemic and have been found only in the type localities: Mopsechiniscus imberbis (Richters, 1907) from South Georgia, sub-Antarctic (Richters, 1907, 1920; Ottesen and Meier, 1990); Mopsechiniscus franciscae from Victoria Land, Antarctica (Guidetti et al., 2014); Mopsechiniscus tasmanicus Dastych and Moscal, 1992 from Tasmania, Australia (Dastych and Moscal, 1992); and Mopsechiniscus frenoti Dastych, 1999, from the Île de la Possession, Crozet Islands, sub-Antarctic (Dastych, 1999c). Mopsechiniscus schusteri Dastych, 1999 has been reported from Venezuela (Grigarick et al., 1983; Dastych, 1999a) and Costa Rica (Kaczmarek et al., 2014); and Mopsechiniscus granulosus Mihelčič, 1967 has been reported from several Argentinean localities (Mihelčič, 1967, 1971/72; Binda and Kristensen, 1986; Kristensen, 1987; Rossi and Claps, 1989; Dastych, 2000; Rossi et al., 2009; Roszkowska et al., 2016) and Chile (Ramazzotti, 1962; Dastych and Moscal, 1992; Dastych, 2000). According to Dastych (1999a, 2001), there are two more undescribed new species from Brazil (Du Bois-Reymond Marcus, 1944), and Chile. The distribution of Mopsechiniscus species point to a Gondwanan distribution for the genus, as has already been hypothesized (Dastych and Moscal, 1992; Dastych, 2001).
However, ecological data on Mopsechiniscus species are very limited (see Dastych, 2001). The species of this genus have been found in moss and lichens, rarely liverworts, at different altitudes. An association with environments rich in Nothofagus forests has also been noted (Ramazzotti, 1962; Kristensen, 1987; Dastych & Moscal, 1992). In sub-Antarctic islands, Mospechiniscus was found at 70-700 m a.s.l., in Tierra del Fuego at ca. 1000 m (above the tree line), in subtropical and/or cloud forest from 50 m up to 2000 m, suggesting a mountain and/or subpolar character of the genus (Dastych, 2001). The Antarctic species (M. franciscae) used in this study was found in a large patch of moss growing on gravel soil in a very small valley at Crater Cirque (Guidetti et al., 2014), while the South American species (M. granulosus) was collected at Angol in Chile, though the original substrate was not reported (Jørgensen et al., 2011).
Mopsechiniscus in Antarctica
Three scenarios could account for the presence of Mopsechiniscus in Antarctica, in addition to South America: 1) an early ancestor and speciation occurring early during the initial break-up of Gondwana (ca. 150 Mya); 2) speciation occurring after the break between Antarctica from South America (ca. 30 Mya); 3) recent colonisation via zoogenic introduction (e.g. penguins or sea birds), wind dispersal, and/or anthropogenic activities.
At the species level, modern molecular methods have revealed a remarkable level of endemism of the Antarctic biota, questioning the widespread assumption that small organisms are likely to be ubiquitous and the taxa to which they belong species poor (Chown and Convey, 2007). Recent molecular analyses showed that most Antarctic tardigrades appear to be locally endemic, with a greater diversity than had previously been considered. There were also potentially undescribed species, and a lack of connectivity between most Operational Taxonomic Units from continental Antarctica and those from other Antarctic geographical zones (Velasco-Castrillón et al., 2015). Endemism is very high for maritime and continental Antarctic tardigrade species (more than 80%), with less than 3% of the species in common with taxa from South America, and even fewer when comparing only continental Antarctic species (McInnes, 1994; Velasco-Castillo et al., 2014; Kaczmarek et al., 2015). Some species, e.g. Acutuncus antarcticus (Richters, 1904) and Milnesium antarcticum Tumanov, 2006, are widespread across continental Antarctica, while others have a very limited distribution within this continent (Sohlenius and Boström, 2005; Velasco-Castrillón et al., 2015; Cesari et al., 2016).
This situation is not limited to tardigrades, but occurs also in other representatives of the terrestrial meiofauna with cryptobiotic adaptations, like nematodes and rotifers. These animals show a very similar distribution pattern, e.g. all Victoria Land nematodes are endemic to Antarctica, and many are common and widely distributed at landscape scale (Adams et al., 2014). For rotifers, the level of endemism in Antarctica is 95% of the species, higher than any other continent, with many bdelloid species occurring only in maritime or continental Antarctica (Iakovenko et al., 2007). Molecular studies showed a widespread range for some rotifers in continental Antarctica, but only one bdelloid lineage from continental Antarctica was also present in maritime Antarctica, and no close similarities were found with worldwide locations, or between Antarctic Peninsula and Tierra del Fuego (Argentina) (Velasco-Castrillón et al., 2014).
Based on these findings, anhydrobiotic metazoans living in Antarctica (i.e. tardigrades, nematodes, and rotifers) show a restricted distribution, with high percentage of endemic Antarctic taxa, in spite of their potential for high dispersal. Therefore, it is extremely unlikely that the high number (33) of endemic tardigrade species in Antarctica (including two endemic genera) are the result of speciation after recent colonisation. The literature portrays a very limited and/ or endemic distribution for Mopsechiniscus species, and for continental Antarctica a very reduced presence of echiniscids. This information implies a relatively low dispersal capability for these taxa and, therefore, few possibilities for recent colonisation events. Although, it cannot be excluded, the third scenario, a recent colonisation of Antarctica, is very unlikely for Mopsechiniscus species. If the presence of M. franciscae in Antarctica was the result of a recent colonization, this event would have to be considered extremely rare as no other tardigrade species reported from continental Antarctica have been recorded elsewhere in the world, the exception being a single record (to be confirmed) of A. antarcticus (the most common and widespread Antarctic tardigrade species) in Tierra del Fuego (Claps et al., 2008).
According to the molecular clock, the origin of the genus Mopsechiniscus can be placed somewhere between the origin of its phylogenetic line (i.e. when it separated from its sister taxon; 146–136 Mya) and the split between M. franciscae and M. granulosus (47.8–32.1 Mya) (Table 2). This is after Gondwana separated from Laurasia (ca. 200–180 Mya), but before the complete breakup of Gondwana (ca. 50–30 Mya). This time frame for the origin of the genus and the current distribution of Mopsechiniscus species (Fig. 1; see above) indicate a Gondwanan presence of the genus during the Mesozoic period.
If a more anterior time for the origin of Mopsechiniscus is chosen, e.g. close to the lower limit of the 95% HPD (294 Mya), then the genus would have been extant during the period of existence of the super-continent Pangea (from about 300 Mya until its breakup about 180 Mya). In this scenario, the distribution of the genus would have to have been confined to the Gondwana region of the Pangea throughout the 120 My of super-continent’s duration. A later time for the origin of Mopsechiniscus, e.g. close to the upper limit of the 95% HPD (3 Mya), would require a very late colonisation of three continents and a subsequent rapid speciation within the genus. Again, not the most parsimonious option. According to Dastych (2001), and as discussed above, Mopsechiniscus represents a Gondwanan faunal element with a distribution pattern that is a result of historical factors and subsequent speciation, rather than purely dispersal events.
Our two main analyses (Tables 2, 3) and those used for model comparison (Table 1) returned congruent mean estimates, falling within a time range of 48-32 Mya, for the split between the Antarctic and the South American Mopsechiniscus lineages. This is compatible with the estimated separation of Antarctica and South America (e.g. Livermore et al., 2005), in which the opening of the Drake Passage prevented exchanges of organisms by land and reduced the dispersal ranges of species. The strongly debated estimate for the origin of this passage ranges approximately from 50 to 20 Mya, but in most cases not earlier than the cooling period that followed the Eocene/Oligocene boundary (33.7 Mya; Livermore et al., 2005). Recent geological studies also indicate that the Drake Passage opening is older than 28.5 Mya (Dalziel et al., 2013). Estimates for the general break-up of Australia, Antarctica and South America derived from a molecular clock analysis on Nothofagus, the southern beech with a Gondwanan distribution (Zhang, 2011), provided a range of 50–30 Mya (Cook and Crisp, 2005). All these independent studies on the dating of the geological events that separated Antarctica from South America indicate a time similar to our results for the separation of the respective Mopsechiniscus lineages.
Therefore, our molecular clock analyses support vicariance for the M. franciscae speciation caused by the separation of Antarctica and South America. The scenario of recent dispersal and re-colonisation is very unlikely, as stated previously, but due to the high 95% HPD range alternative scenarios cannot be excluded.
Interestingly, the proposed permanent glaciation of Antarctica at 34 Mya (Scher and Martin, 2006) could have accelerated the geographic isolation of Mopsechiniscus populations; the reduction of the available habitats increased the distance between, and reduced the number of, populations, with clear consequences for the subsequent speciation process. Therefore, the allopatric speciation of Antarctic tardigrades could be the consequence of two geographical separation/ isolation promoting events: the separation between Antarctica and South America and the glaciation of Antarctica.
If our hypothesis is correct, the vicariance events have separated the Mopsechiniscus lineages and isolated M. franciscae (and possibly other tardigrade endemic species) in Antarctica, implying that this species represents a relict faunal fragment that survived the Last Glacial Maximum (LGM; ca. 20,000 years ago). Even the lower 95% HPD limit (3 Mya) for the origin of the Antarctic Mopsechiniscus lineage would indicate a long presence in Antarctica, and the consequent survival through the extreme conditions present during the LGM.
Other possible scenarios for the presence of M. franciscae in Antarctica cannot be excluded, although we consider them unlikely for the reasons explained above. As M. franciscae is the only Mopsechiniscus species identified in Antarctica, other speciation processes (e.g. sympatric or parapatric speciation) are very improbable. In principle, a recent colonization of Antarctica by M. franciscae either from unexplored regions or by another Mopsechiniscus species followed by speciation is possible. Both scenarios would imply a high dispersal capability and a wide distribution outside Antarctica; two characteristics for which there is currently no evidence, and therefore should be considered improbable. The presence of M. franciscae in Antarctica could represent the result of regional extinctions outside Antarctica, or of other Mopsechiniscus species (e.g. M granulosus) within Antarctica. This scenario would suggest the coexistence of more than one Mopsechiniscus species in an area, a situation that has never been reported.
Mopsechiniscus in the sub-Antarctic islands
The presence of Mopsechiniscus on two sub-Antarctic islands is intriguing. South Georgia, where M. imberbis is found, is recognised as a micro-continent that has geological links with the Patagonian Andean Mountains, situated to the east of the Beagle Channel and attached to the southern margin of the Burdwood Bank (Dalziel et al., 1975). There is some debate over the positioning and subsequent movement of this micro-continental plate during the late Cretaceous-early Paleogene period (Dalziel et al., 1975; Barker, 2001; Thomson, 2004). Lawver and Gahagan (2003) provide a computerised continental break-up history of whole Antarctica, placing South Georgia to the south of Burdwood Bank and in close proximity to Tierra del Fuego. With the addition of our results for the estimated molecular clock division between two phylogenetic lineages (the Antarctic M. franciscae and the South American M. granulosus), the latter scenario is congruent with the hypothesis that Mopsechiniscus was present on South Georgia before it broke away from Tierra del Fuego.
Mopsechiniscus frenoti of the Crozet Islands is morphologically very similar to M. franciscae from Antarctica (Guidetti et al., 2014) and, based on the available data, we can infer that the two species represent sister taxa within the genus. The volcanic rocks of the sub-Antarctic Crozet archipelago have a relatively recent origin (ca. 8.8 Mya; Giret et al., 2003). However, the origins of the islands on the Crozet Plateau are debated (see Craig, 2003). Suggested interpretations of palaeogeographic data put these islands near India, close to Madagascar or off Antarctica over a period between late Cretaceous (ca. 70 Mya) to the Palaeocene (60–63 Mya) (Craig, 2003). The Crozet Islands host a number of indigenous species including plants, carabid beetles, and black flies (Chown et al., 1998; Vernon et al., 1999; Craig et al., 2003). How these indigenous flora and fauna, and indeed Mopsechiniscus, reached the islands is unknown. Winds and birds are potential vectors, especially as the Crozet Islands would have been formed 1,000 km closer to Africa during the Palaeocene (Schlich et al., 1974), but there is no evidence that passive long distance dispersal is common for Mopsechiniscus.
It is entirely possible that Mopsechiniscus species indigenous of South Georgia and the Crozet Islands could also be present in localities we have not yet discovered. Alternatively, they may have become isolated on the islands by traversing land/island bridges that have by now vanished.