Biogeography of circum-Antarctic springtails

Abstract

We examine the effects of isolation over both ancient and contemporary timescales on evolutionary diversification and speciation patterns of springtail species in circum-Antarctica, with special focus on members of the genus Cryptopygus (Collembola, Isotomidae).

We employ phylogenetic analysis of mitochondrial DNA (cox1), and ribosomal DNA (18S and 28S) genes in the programmes MrBayes and RAxML. Our aims are twofold: (1) we evaluate existing taxonomy in light of previous work which found dubious taxonomic classification in several taxa based on cox1 analysis; (2) we evaluate the biogeographic origin of our chosen suite of springtail species based on dispersal/vicariance scenarios, the magnitude of genetic divergence among lineages and the age and accessibility of potential habitat.

The dubious taxonomic characterisation of Cryptopygus species highlighted previously is confirmed by our multi-gene phylogenetic analyses. Specifically, according to the current taxonomy, Cryptopygus antarcticus subspecies are not completely monophyletic and neither are Cryptopygus species in general. We show that distribution patterns among species/lineages are both dispersal- and vicariance-driven. Episodes of colonisation appear to have occurred frequently, the routes of which may have followed currents in the Southern Ocean. In several cases, the estimated divergence dates among species correspond well with the timing of terrestrial habitat availability.

We conclude that these isotomid springtails have a varied and diverse evolutionary history in the circum-Antarctic that consists of both ancient and recent elements and is reflected in a dynamic contemporary fauna.

Introduction

Antarctic terrestrial ecosystems are structured by many of the same forces that influence evolution elsewhere; however, the importance of isolation and its subsequent effects on population and species differentiation is perhaps easier to appreciate on the continent locked in ice. In Antarctica, previous glacial cycling and current dispersal barriers (e.g. glaciers) play a role in defining the limits of distribution of different species, but other less obvious forces are also important (Rogers, 2007). For example, ecological properties such as availability of liquid water and ice-free soil are variable, and patchiness in available habitat is likely to influence population structure. Intrinsic characteristics of Antarctic terrestrial biota such as microarthropods include an absence of wings, limited desiccation tolerance and reduced body size. Since these characteristics are likely to have marked effects on dispersal capabilities of such taxa, they are also likely to strongly influence population structure over time. Collectively, glaciological/ecological forces and species life history traits are therefore likely to have dominated and defined evolutionary processes in Antarctic terrestrial taxa through their isolating effects (e.g. Frati et al., 2001, McGaughran et al., 2008). In this context, the patchily distributed springtails of Antarctic terrestrial ecosystems are good candidates for studies of the mechanisms of evolutionary processes such as speciation.

To date 25 springtail species have been described in Antarctica (Greenslade, 1995), with most genera belonging to the Isotomidae, members of which are also widely distributed globally (Frati and Carapelli, 1999). Antarctic springtail distribution and taxonomy received considerable attention in the 1960s and early 1970s (e.g. Gressitt et al., 1963, Wise and Gressitt, 1965, Gressitt, 1967, Strandtmann, 1967, Wise, 1967, Wise, 1971, Wise and Spain, 1967, Wise and Shoup, 1971). However, phylogenetic classification among globally distributed springtails has been a subject of disagreement among various authors (e.g. D’Haese, 2002, D’Haese, 2003, Xiong et al., 2008) and Antarctic species have received little attention in this context (Frati et al., 2000). In fact, only one paper (based on mitochondrial DNA (mtDNA) cox1 variation) has examined phylogenetic relationships within Antarctic Isotomidae (Stevens et al., 2006).

This work examined several southern hemisphere isotomid springtails, paying particular attention to the genetic relationships among Cryptopygus species (Stevens et al., 2006). These authors found that several isotomid species were dubiously classified, collectively forming a non-monophyletic group. In fact, several morphologically recognisable but currently undescribed Cryptopygus species clustered into paraphyletic sister relationships with described Antarctic species (Stevens et al., 2006). An additional key finding of Stevens et al. (2006) was that some biogeographically separate locations harboured species with shallow divergence (<2 MA), while other species showed deeper genetic divergences (>10 MA). This suggests that springtail taxa in Antarctica may have variable evolutionary origins.

Antarctica is essentially a conglomerate of distinct regions encompassing the sub-, maritime- and continental-Antarctic. However, even regions within the continent are now recognised as discrete biogeographical elements (Chown and Convey, 2007). For example, the eastern and western parts of the Antarctic continent are very different (Chown and Convey, 2007) and at finer scales, no springtail species are shared across Antarctica’s “Gressitt Line” – a divide between continental-Antarctica and the Antarctic Peninsula (Chown and Convey, 2007, Torricelli et al., 2010) (see Fig. 1).

The springtail fauna of Antarctica includes a high proportion of endemic genera. For example, of the 10 species in eastern Antarctica (six of which are from the family Isotomidae; Sinclair and Stevens, 2006), 60% of genera and all species are endemic (Wise, 1967, Wise, 1971, Greenslade, 1995, Stevens and Hogg, 2006, Pugh and Convey, 2008, Torricelli et al., 2010). The high occurrence of Antarctic endemics is often taken as evidence of divergence in isolation, suggesting survival of these groups through ancient times (Stevens et al., 2006, Convey and Stevens, 2007, Rogers, 2007, Convey et al., 2008, Convey et al., 2009). In the context of Antarctic phylogeography, recent mtDNA work has confirmed that some species show divergence/speciation over multi-million year timescales (e.g. Stevens et al., 2007, McGaughran et al., 2008, McGaughran et al., 2009). Alternatively, non-endemic species with wider cosmopolitan distributions are generally presumed to represent more recent introductions.

These concepts – ‘divergence in isolation’ and ‘recent introduction’ – largely correspond to two evolutionary processes that are often invoked to explain distribution patterns and the genetic relationships among species. These are fragmentation of ancestral populations by vicariant events or colonisation of new areas by dispersal across a pre-existing barrier (Sanmartín and Ronquist, 2004). In general terms, taxa are expected to have either: (1) survived environmental conditions in Antarctica since the break-up of Gondwanaland and subsequent settlement of the major southern landmasses (Lawver et al., 1992, Crame, 1999, Convey et al., 2008, Convey et al., 2009) over 30 MA (i.e. vicariance origin) or (2) dispersed to Antarctica in more recent times (<5 MA; dispersal origin) following currents in the Southern Ocean (e.g. the Antarctic Circumpolar Current (ACC), the West Wind Drift (WWD); Williams et al., 2003, and references therein). Of course, taxa may have dispersed to Antarctica in ancient times and then undergone vicariant fragmentation of populations. Additionally, palaeoclimatic changes (including very recent Pleistocene (<2 MA) climatic cycles) may have caused vicariance patterns among populations in more recent times (Clarke and Crame, 1992).

Variable habitat has been available across a variety of timescales in the southern hemisphere for vicariant (fragmentation) and/or dispersal (colonisation) processes. In addition to the ancient ‘Gondwanan’ landmasses (continental-Antarctica, Australia, New Zealand, South America), sub-Antarctic Îles Crozet (∼8.7 Myr) and Îles Kerguelen (∼100 Myr) have had available habitat over the long-term. Elsewhere in the Southern Ocean, islands such as Heard, Macquarie and Marion Island, and coastal regions of the Antarctic Peninsula have all become available within the last million years. Thus, contemporary species distributions most likely reflect a varied origin for Antarctic springtails (Frati and Carapelli, 1999) that includes both relic and more recent immigrant species (e.g. Wallwork, 1973, Greenslade, 1995, Marshall and Pugh, 1996, Marshall and Coetzee, 2000, Pugh and Convey, 2000) and the age of available habitat is likely to have been a key component in the overall structuring of contemporary lineages.

To examine this more closely, we significantly extend the work of Stevens et al. (2006) outlined above. Our first aim is to evaluate existing taxonomy of a suite of species of the springtail family Isotomidae from Antarctica and circum-Antarctic locations in light of the dubious taxonomic classifications identified in several taxa by Stevens et al. (2006). We do this by adding several new individuals/locations to the existing cox1 dataset, and combining analyses of maternally inherited mtDNA (cox1) with bi-parentally inherited nuclear (18S and 28S rDNA) genes. We are particularly interested to see if our expanded dataset confirms/refutes the paraphyly of Cryptopygus species identified by Stevens et al. (2006). Our second aim is to evaluate the biogeographic origin of the genus Cryptopygus by using dating estimates and dispersal–vicariance (DIVA) analysis. We hypothesise that the Cryptopygus taxa will show a dynamic evolutionary origin that includes both dispersal and vicariant-based episodes. In addition, we hypothesise that the blend of both shallow and deeply diverged Cryptopygus species identified by Stevens et al. (2006) will correspond to certain geographical constraints (i.e. age of available habitat). In particular, we predict that species found in younger habitats (or habitats that have become available more recently) will correspondingly be home to lineages that have diverged/speciated more recently, and that older less penetrable regions will harbour more deeply diverged lineages that have survived a long evolutionary period in isolation (see location colour codes in Fig. 1).