Contributions to Zoology, 86 (2) – 2017Roberto Guidetti; Sandra J. McInnes; Michele Cesari; Lorena Rebecchi; Omar Rota-Stabelli: Evolutionary scenarios for the origin of an Antarctic tardigrade species based on molecular clock analyses and biogeographic data

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Introduction

The biogeographic origins of the extant limno-terrestrial fauna of maritime and continental Antarctica, and the sub-Antarctic islands have been debated for more than a decade (e.g. Pugh and Scott, 2002; Barnes et al., 2006; Convey et al., 2007, 2008; Pugh and Convey, 2008; Convey, 2010; Vyverman et al., 2010; Fraser et al., 2012). The current biogeographic distributions of Antarctic endemic or circum-Antarctic taxa could be the result of recent, ongoing dispersal in Antarctic regions (re-colonisation hypothesis; see Pugh, 2004) and/or the consequence of relict Gondwanan taxa surviving the extreme, harsh conditions of Antarctica over the last 23 million years (My) (glacial refugia hypothesis; see Stevens et al., 2006). In the latter case, the extant fauna would be represented by ancient endemic taxa or new more recent taxa that evolved in situ from populations that had survived in ice-free refugia.

Antarctica formed a major component of the Gon­dwanan continent with a rich fauna and flora before geological and climate evolution isolated the continent and successive ice ages eliminated most plant and animal life. The extant biota that might have been associated with that period has been restricted to cryptogams and terrestrial meiofauna (Convey, 2010). Tardigrades, rotifers, and nematodes are major components of terrestrial Antarctic meiofauna in terms of diversity, number of specimens, distribution, and colonised substrates. Antarctic terrestrial biota are often characterised by high endemism (Chown and Convey, 2007) and it has been hypothesised that long-term glacial habitat fragmentation and the consequent in situ isolation of biota was a likely cause (Stevens and Hogg, 2003, 2006).

Identifying biogeographic patterns and hypothesising species evolutionary origin are difficult tasks that require a combination of scientific disciplines and appropriate models. Understanding the origin and evolution of specific Antarctic biota requires finding particular taxa with clear biogeographic distributions. A fundamental element for investigating evolutionary biogeographic patterns is the definition of a temporal framework. Recent advances in molecular studies have provided novel chronological approaches in the form of molecular dating (a.k.a. molecular palaeobiology, or molecular clocks), which uses molecular and palaeontological analyses to provide a temporal framework. This framework can be used to explain evolutionary and geological events (Rota-Stabelli et al., 2013), and to test alternative biogeographic hypotheses.

Mopsechiniscus franciscae Guidetti et al., 2014 was recently discovered in Victoria Land, Antarctica (Guidetti et al., 2014; Fig. 1), and represents one of the only three heterotardigrade species found in continental Antarctica. This new discovery, led us to evaluate the utility of this genus as a model taxon to test evolutionary patterns and biogeographical history within the timeframe of key Antarctic geological events. Mopsechiniscus is one of the few Echiniscidae for which there are molecular studies for more than one species (Jørgensen et al., 2011; Guidetti et al., 2014). Mopsechiniscus franciscae possesses the capability of cryptobiosis, which enables most limnic and terrestrial tardigrades to tolerate harsh climate conditions, such as those present in Antarctica (for reviews see Guidetti et al., 2011; Møbjerg et al., 2011; Wełnicz et al., 2011). This capability, coupled with their small body size (< 1 mm), may have provided tardigrades with a high advantage for dispersal and colonisation of Antarctica. However, until now, long distance dispersal has been demonstrated for a few terrestrial species only (Jørgensen et al., 2007; Cesari et al., 2009, 2016; Bertolani et al., 2011; Guidetti et al., 2016), and based on the limited distribution of most taxa, the tardigrade capability for long distance dispersal has been questioned (McInnes and Pugh, 1998; Pilato and Binda, 2001). Such as co-occurring micro-arthropods, Antarctic tardigrade distribution could represent a fauna comprising disjunct relicts (Marshall and Pugh, 1996; Pugh and Convey, 2000) or be the products of post-glacial speciation (Stevens and Hogg, 2003).

In order to shed new light on the origin and geo-chronology of the Antarctic continental fauna, we explored possible evolutionary scenarios for the origin of a component of the Antarctic meiofauna (i.e. the tardigrade M. franciscae) using molecular dating analyses and historical biogeography.

FIG2

Fig 1. a Scanning electron micrograph of the heterotardigrade Mopsechiniscus franciscae. b Geographical distribution of the living species of Mopsechiniscus known to date (spots). 1 = Mopsechiniscus franciscae, Victoria Land, Antarctica; 2 = Mopsechiniscus imberbis, South Georgia, Sub-Antarctic Islands; 3 = Mopsechiniscus frenoti, Crozet Islands, Sub-Antarctic Islands; 4 = Mopsechiniscus tasmanicus, Tasmania, Australia; 5 = Mopsechiniscus sp., Chile; 6 = Mopsechiniscus granulosus, Argentina; 7 = Mopsechiniscus granulosus, Chile; 8 = Mopsechiniscus sp., Brazil; 9 = Mopsechiniscus schusteri, Venezuela; 10 = Mopsechiniscus schusteri, Costa Rica.