Australia is an old and weathered continent, with subdued topography and few major physical barriers. Since the early Eocene, global climatic shifts associated with polar ice-sheet growth and decay have dramatically changed the landscapes and biomes across the continent (Fujioka & Chappell, 2010). Tropical forests that dominated the central interior have long since disappeared, replaced by vast deserts of an arid regime established in the mid- to late Miocene, and reaching its peak during the glacial cycles of the Pleistocene (Flower & Kennett, 1994). Much like the spread of ice sheets across the Northern Hemisphere, desertification of the Australian interior would have resulted in significant geographical displacement of temperate-adapted taxa, and undoubtedly had a profound effect on the composition and diversification of the Australian biota (reviewed in Byrne et al., 2008).
The Australian landmass is dominated by a relatively homogeneous central arid zone surrounded by a periphery of wetter biomes that often are separated by arid corridors. The historical fragmentation and isolation of these biomes had important evolutionary consequences, and recognition of a distinctive fauna and flora has led to the delimitation of a number of areas of endemism across Australia (e.g. Cracraft, 1991; Unmack, 2001). While fine-scale patterns of diversity and evolutionary history have been well studied in areas such as the rain forests of north-eastern Queensland (e.g. Bell et al., 2010), and the temperate forests of south-western (e.g. Kay & Keogh, 2012) and south-eastern Australia (e.g. Chapple et al., 2011), other regions, particularly arid parts of the continent, have received comparatively little attention (Byrne et al., 2008).
The Pilbara region in remote north-western Western Australia is one of the oldest land surfaces on Earth (Pillans, 2007). Bound by the Indian Ocean to the west, vast sand deserts to the north and east, and highly metamorphosed rocks to the south, it has long been regarded as one of Australia's centres of biological endemism (Cracraft, 1991), and has a landscape so different from surrounding regions it can be identified from space (Fig. 1a). Situated in what is presently part of Australia's vast arid zone, the Pilbara has preserved in its unique and ancient sediments a rich and complex history: marine structures in the form of a 3.43 billion-year-old stromatolite reef (Allwood et al., 2007); immense glacial scarring from the Permo-Carboniferous ice age (Gale, 1992); numerous palaeochannels reflecting past, wetter hydrological regimes (Macphail & Stone, 2004); and the richest concentration of indigenous rock art in the world (Environmental Protection Authority, 1995).
While the Pilbara is well known to harbour a unique biota (Cracraft, 1991; Unmack, 2001), comparatively little is known of the evolutionary history of the flora and fauna that inhabit the region. Inadequate fine-scale sampling in the remote area has limited phylogeography-based studies, and existing phylogenies typically use only a small number of Pilbara samples to place the broader Pilbara region in context with other areas of endemism. However, a recent comprehensive survey of biodiversity has collected and catalogued a wealth of biological material, along with detailed records of habitat and physical landscape across the entire region (McKenzie et al., 2009). The enormous potential of these data for future work warrants an assessment of what is currently known about the Pilbara. Here we review the geophysical and climate history of the region to lay the foundations upon which hypotheses regarding the evolution of the unique Pilbara fauna can be outlined, refined and tested. We evaluate patterns emerging from previous studies of Pilbara biota, both in the broader context of the arid zone, and also how they relate to the distribution of major geo- and biophysical units across the Pilbara itself. We then assess alternative biogeographical scenarios using a molecular phylogenetic approach based on multiple gecko taxa, to shed light on the relationship between biotic diversification and the evolution of the Pilbara landscape.
Defining the Pilbara region
The precise region(s) encompassed by the name ‘Pilbara’ differ in extent and/or definition depending on the expertise and interests of the authors involved. For example, the ‘Pilbara district’ refers to the broad area generally known as the ‘north-west’, and lies north of latitude 25°00′ S and west of longitude 121°30′ E, including the coastline from Shark Bay to Eighty-Mile Beach (Beard, 1975). More specifically, the ‘Pilbara biogeographical region’ is defined by a number of major attributes including climate, geology, landform and vegetation (Thackway & Cresswell, 1995) and corresponds with the ‘Fortescue botanical district’ of the Eremaean Province (Beard, 1990). For geologists, the ‘Pilbara craton’ refers to the ovoid, plateaued and rugged region distinguished by surface outcrops of ancient rocks (see below). Given that the boundaries of the Pilbara biogeographical region and the Fortescue botanical district closely follow the geological boundary of the Pilbara craton, this particular region specifically will be referred to as the ‘Pilbara’, as differentiated from the broader ‘Pilbara district’.
The Pilbara is a distinct geological entity, so different from surrounding regions that it is visible in satellite imagery. The region is defined by underlying sedimentary and igneous rocks of the Pilbara craton ranging up to 3.72 billion years (Ga) in age, and is overlain by one of the most ancient erosion surfaces on Earth (Geological Survey of Western Australia, 1990; Myers & Hocking, 1998). The craton can be divided into two parts; heavily weathered Archaean (3.72–2.85 Ga) granites and metamorphosed volcanic rocks (‘greenstones’) forming undulating hills and plains in the north, and stratigraphically overlying these rocks in the south is a group of younger (2.77 to 2.40 Ga) Archaean to Proterozoic basalts, and iron-rich sedimentary rocks deposited in the Hamersley Basin (Van Kranendonk et al., 2002) (formally named the Mount Bruce supergroup; Trendall, 1995; Fig. 1b). A comprehensive summary of the different geological formations and their landform expression can be found in Beard's (1975) description of the Pilbara's natural regions. For more detailed information on the structure and tectonic development of the craton see Myers (1993), Trendall (1995) and Van Kranendonk et al. (2002).
Much younger terrains of unmetamorphosed sedimentary rocks surround the Pilbara craton to the north and east, and these are overlain by topographically homogeneous sand deserts that dominate the arid interior of Australia. To the south, however, the rocky terrains of the Pilbara extend into rocky landscapes of the geological entity known as the Capricorn Orogen (and associated Gascoyne Complex). This region is composed of folded, faulted and highly metamorphosed rocks, and reflects the ancient collision and amalgamation of the Pilbara and adjacent Yilgarn craton (Myers, 1993).
The Pilbara landscape is topographically variable and largely determined by underlying geological structures. The rugged ranges of the Pilbara comprise ridges and mountains that generally are associated with the rocks of the Hamersley Basin in the southern part of the craton. The most noticeable topographical elements of this region are the plateaus of the iron-rich Hamersley and basaltic Chichester Ranges that traverse the craton roughly east–west, and reach elevations of around 900 (and up to 1250) and 600 m a.s.l., respectively. In addition, the Fortescue River valley dissects the Hamersley Basin east to west, and consists of alluvial plains in the east, and deeply incised gorge systems in the central and western parts of the drainage. This formidable land feature not only divides the rocky landscapes on either side of the river valley, but provides a distinct habitat itself based on the sand/clay/silt substrates of the valley floor (McKenzie et al., 2009). The northern part of the craton is much more topographically subdued, due to the highly weathered nature of the granite/greenstone terrains. This region is characterized by low hills and alluvial plains, which are traversed by numerous flood channels of the Oakover, DeGrey, Coonan, Shaw, Yule and Turner rivers (see Reeves et al., 2007). The northern part of the craton can be divided into a number of distinct landforms represented in the ‘natural regions’ of Beard (1975), and these appear to correlate with distinct structural elements of the underlying geology (see Van Kranendonk et al., 2006; and Allwood et al., 2007). For example, there is a strong east–west division separating the Abydos Plain of Beard (1975) (correlating with the underlying De Grey Superbasin; Van Kranendonk et al., 2006), and the Oakover Valley (and associated underlying East Pilbara Terrain). A gently sloping coastal plain has developed along the north-western Pilbara. For a detailed review of the physiography of the region, see Beard (1975) and Johnson (2004).
Although geologically distinct, some of the landscapes surrounding the Pilbara craton are similar to those found within the Pilbara. For example, sandy areas of the coastal plain resemble those of the adjacent Great Sandy and Little Sandy deserts, and also the Carnarvon coastal plain to the south of the craton. Furthermore, rocky substrates like those that characterize the southern Pilbara are also found throughout the Capricorn Orogen to the south, although here they are less extensive than within the craton.
Vegetation and bioregions
The richness of regional habitats and vegetation types often is a measure of geological diversity, and this is exemplified in the Pilbara. The extensive river systems and deeply excised gorges, aquifer-fed springs and wetlands, flat coastal plains and razor-backed ridges all contribute to the heterogeneous nature of the Pilbara landscape that, as mentioned above, is shaped to a large degree by underlying geological substrate. At the regional scale, biogeographical patterns can be seen across the Pilbara that broadly reflect the geological and physiographical units of the craton. Using information from a combination of geology, landform, climate, vegetation and animal communities, the Pilbara has been divided into four geographically distinct subregions [Interim Biogeographic Regionalisation for Australia (IBRA); Environment Australia, 2008] (Fig. 1c). The Hamersley subregion comprises the southernmost portion of the Hamersley Basin and encompasses the Hamersley Range. This region is characterized by skeletal soils developed on the iron-rich sedimentary rocks, and generally consists of spinifex grassland with mulga and snappy gum (tree steppe) (Beard, 1975). The Chichester subregion encompasses the granite/greenstone terrains of the northern craton but also includes the Chichester Plateau of the Hamersley Basin. Beard (1975) defined a number of subdivisions within the northern craton (see above), reflecting substantial landscape heterogeneity across this broad area. While the broader Chichester subregion is characterized by deeply weathered regolith and is dominated by spinifex (Triodia spp.) grassland with irregularly scattered shrubs (shrub steppe), the Chichester Plateau (bordering the northern side of the Fortescue Valley) more closely reflects the soil landscape and vegetation of the Hamersley Plateau (Tille, 2006). The Fortescue Plains subregion is delineated by the Fortescue River valley, which cuts through the sedimentary rocks of the Hamersley Basin. This region consists of salt marshes, mulga-bunch and short grass communities, with eucalyptus (Eucalyptus spp.) woodlands along the permanent springs. Finally, the Roebourne subregion encompasses the mudflats and low dunes of the coastal plain and is composed largely of alluvial and aeolian sediments, often with a cover of grasses and soft spinifex. Detailed descriptions of the subregions can be found in McKenzie et al. (2009) and are summarized in Guthrie et al. (2010). In addition, the soil landscapes of the Pilbara have been mapped and described in detail by Tille (2006).
The IBRA bioregions surrounding the Pilbara (i.e. Carnarvon to the south-west, Gascoyne to the south, and the Great Sandy and Little Sandy deserts to the east) differ in climate, landform, geology and soil, and therefore comprise different vegetation associations (Beard, 1969, 1975, 1990).
A stable refuge amidst changing climates
The landscapes of the Pilbara have been subaerially exposed since the Pre-Cambrian (> 540 Ma) (Pillans, 2007). During this time, vastly different climatic regimes have come and gone, and the region has been greatly modified, with extensive glaciers during the Permo-Carboniferous ice age carving valleys into the Pilbara plateau, and aiding the erosion of more than 700 m from the mountains (Taylor, 1994). During its more recent history, and the timeframe of relevance to studies of the modern biota, vast changes have occurred across areas surrounding the Pilbara. However, largely due to its topographical heterogeneity and proximity to the coast, the Pilbara (or more likely, localized regions within the Pilbara) would have sustained more thermally buffered environments compared to the lower-lying, homogeneous landscapes that comprise much of the arid zone (Macphail & Stone, 2004; Byrne et al., 2008), allowing the persistence of mesic-adapted taxa (Oliver et al., 2010; Pepper et al., 2011a,b,c).
Excellent descriptions of the palaeohistory of landforms in Australia, including the Pilbara, can be found in Wasson (1982) and Taylor (1994), therefore below we present a brief summary of events that have contributed to the isolation of the Pilbara in more recent times. The mid-Cretaceous (c. 100 Ma) saw the chain of basins to the east of the Pilbara inundated by shallow oceans, separating the Archaean rocks of the Pilbara craton from their exposures in the Kimberley and central Australia. Sea-level transgressions and regressions during the Cretaceous saw the basins oscillate between non-marine and open-water conditions, and would have had a significant impact on spatial and habitat diversity in the area (Wasson, 1982). Changes in sea level along the continental shelf also periodically connected offshore islands such as those in the Dampier Archipelago, most recently during the Last Glacial Maximum (Yokoyama et al., 2001). As well as encompassing physical changes to the environment, global oscillations in sea level reflect large-scale variations in climate regimes. Global cooling of sea surface temperatures during the Cenozoic had a profound impact on atmospheric pressure systems and circulation, and on the Australian continent the effect of these changes was the aridification of the continental interior (Frakes et al., 1987). Climate during the Cenozoic in Australia is largely inferred using sedimentological and palaeontological data from southern marginal and inland basins (Fujioka & Chappell, 2010), and a large amount of uncertainty surrounds the onshore palaeoclimate history of the north-west. A chronology of Cenozoic climate and aridification history in Australia can be found in Quilty (1994), Martin (2006), Byrne et al. (2008) and Fujioka & Chappell (2010). Of particular importance during this period, geological and palaeontological records from the middle Miocene provide evidence of the last time drainage and significant vegetation existed in central Australia (Quilty, 1994). Rapid global cooling in the late Miocene led to diminishing precipitation and increasing aridification, with widespread arid conditions thought to be prevalent by the late Miocene (Flower & Kennett, 1994; Fujioka & Chappell, 2010). A temporary return to warm and wet conditions is inferred in the early Pliocene, associated with major sea level rise and basin flooding (Byrne et al., 2008). The height of arid conditions in Australia appears to correlate with the transition from high-frequency, low-amplitude glaciations (every 40 kyr) that characterized the late Pliocene/early Pleistocene, to the low-frequency, high-amplitude glaciations (every 100 kyr) that became established in the middle Pleistocene (Huybers, 2007). This led to increasingly severe aridification and the development of the vast inland sand deserts (Fujioka et al., 2009; McLaren & Wallace, 2010). While a lack of chronological data from Western Australia precludes an accurate age estimate of the Great Sandy, Gibson and Great Victoria deserts, dated playas and dunes in central Australia indicate they probably formed < 1 Ma (Fujioka et al., 2009; Fujioka & Chappell, 2010). The recent development of these vast sand deserts entirely isolated the Pilbara from rocky exposures in central and northern Australia with hundreds of kilometres of dune fields and sand plains.
Biotic elements of the Pilbara
The antiquity and complex geological and climatic history of the Pilbara and surrounds has undoubtedly had a profound influence on the evolutionary history of the flora and fauna that inhabit these regions. Indeed, the distinctive biota has led to recognition of the Pilbara as one of Australia's regional centres of endemism (Cracraft, 1991; Unmack, 2001; Ladiges et al., 2006). A number of studies have attempted to put the Pilbara in context with other areas of endemism, in particular that of Cracraft (1991), who used cladistic biogeographical analyses of a number of vertebrate groups to conclude that, although the precise affinity of the Pilbara to other regions of endemism was uncertain, a close association with the western and eastern deserts was evident. This relationship has been supported by a number of subsequent molecular studies on both plants and animals (Edwards, 2003; Ladiges et al., 2006; Pepper et al., 2006, 2011a,b; Oliver et al., 2010; Catullo et al., 2011; Melville et al., 2011).
While detailed molecular studies of Pilbara biota are in their infancy, the Pilbara appears to be a region of high species diversity, due in part to its long history as a mesic refugium (Oliver et al., 2010; Pepper et al., 2011a,c). In particular, a growing literature is emerging on subterranean invertebrate fauna (Humphreys, 2001; Finston & Johnson, 2004; Eberhard et al., 2005; Karanovic, 2007; Harvey et al., 2008; Finston et al., 2009). These studies suggest that vicariant isolation and divergence due to surface aridification, coupled with underlying geological complexity, have generated astonishing levels of extremely localized diversity, highlighting the Pilbara as a region of global significance (Eberhard et al., 2005). High diversity has also been found in snails (Johnson et al., 2006), and preliminary results from the Pilbara Biodiversity Survey indicate a substantial undescribed flora and terrestrial invertebrate fauna. For example, Guthrie et al. (2010) reports that 68% of beetles collected could not be assigned to recognized species, and Volschenk et al. (2010) could not classify 83% of scorpion morphotypes to described species.
The Pilbara is known to harbour a suite of endemic vertebrates (How & Cooper, 2002; How & Dell, 2004; Gibson & McKenzie, 2009; Doughty et al., 2011a), with studies of widespread arid zone taxa typically revealing morphologically and genetically divergent Pilbara populations (e.g. Baverstock et al., 1983; Painter et al., 1995; Aplin & Donnellan, 1999; Blacket et al., 2000; Pepper et al., 2006; Ford & Johnson, 2007; Oliver et al., 2010; Doughty & Oliver, 2011; Melville et al., 2011). In addition, emerging results from fine-scale molecular studies of terrestrial vertebrates suggest substantial cryptic diversity and complex genetic patterns across the Pilbara landscape (Pepper et al., 2008, 2011a; Shoo et al., 2008; Doughty et al., 2010, 2011b; Catullo et al., 2011).
Spatial heterogeneity within the Pilbara, along with the extensive surrounding deserts, suggests numerous potential physiographical and habitat barriers that may have influenced the evolutionary history of the terrestrial biota. Certainly species richness patterns of both invertebrates and vertebrate fauna have shown a strong correlation with surface type (Durrant et al., 2010; Guthrie et al., 2010; Doughty et al., 2011a). Using comparative, independent datasets of multiple taxa distributed both within and outside the Pilbara, it is possible to assess fine-scale patterns of genetic structuring in relation to the distribution of major landscape types and geodiversity, and in doing so identify potential barriers to dispersal and other abiotic factors associated with diversification.
The vastly dissimilar climate and landforms surrounding the Pilbara are likely to have isolated habitat-specialized fauna following the development of the deserts. For example, the distributions of widespread saxicolous taxa across western, northern and central Australia are often disjunct, reflecting the presence of vast, intervening sand dunes (Ford & Johnson, 2007; Shoo et al., 2008; Oliver et al., 2010; Doughty et al., 2011b; Pepper et al., 2011c). However, arid-adapted taxa distributed throughout the deserts as well as in the Pilbara also exhibit genetic differentiation across the Pilbara margin (Pepper et al., 2006). This suggests potential vicariant isolation, or alternatively diversification driven by habitat specialization (Pianka, 1969; James & Shine, 2000). Sampling other widespread taxa that occur both in the Pilbara and surrounds provides the opportunity to assess whether habitat specificity and/or vicariance has played a role in the differentiation of Pilbara biota on a larger scale. Because some areas of the Pilbara comprise habitats similar to those outside the craton (i.e. the sands of the Pilbara Roebourne coastal plain and those of the adjacent Great Sandy Desert, or the rocks of the Pilbara Hamersley Basin and those of the Gascoyne Bioregion) we might expect taxa with specific habitat preferences to span both regions. However, if multiple taxa exhibit genetic breaks concordant with the boundary of the Pilbara craton irrespective of these largely continuous habitats, it is possible that vicariant isolation and subsequent diversification in response to a presently absent physical barrier (such as ephemeral river systems) were responsible.
Little is known of intraspecific genetic structure of Pilbara vertebrates. Variations in geology, topography and associated habitats are, to varying degrees depending on the taxon, expected to influence the partitioning of genetic diversity across the Pilbara. We assess phylogenetic concordance to broad geographical subdivisions within the Pilbara in order to lay foundations for future studies. Based on existing knowledge of geology and vegetation structure that is widely used in biodiversity assessment of the Pilbara, three simple biogeographical subdivisions are relevant:
Scenario A. The major geological divide separating the northern granite/greenstone terrain (Fig. 1b, red) from the southern Hamersley Basin (Fig. 1b, blue). The results of Pepper et al. (2008) suggested a possible correlation between genetic patterns and underlying geological substrate.
Scenario B. The four IBRA subregions – Chichester (Fig. 1c, pink), Hamersley (Fig. 1c, green), Roebourne (Fig. 1c, yellow) and Fortescue (Fig. 1c, purple) – delimited based on differences in vegetation communities and landsystems across the Pilbara. Importantly, the Chichester Plateau (comprising a major mountain range in the Pilbara), aligned geologically with the southern geological unit of the Hamersley Basin (see scenario A), is considered here as part of the broad northern Chichester subregion in the IBRA regionalization. A number of recent studies have examined invertebrate species compositional patterns in light of these subregions (Durrant et al., 2010; Guthrie et al., 2010; Pinder et al., 2010), as well as vertebrates (Gibson & McKenzie, 2009; Doughty et al., 2011a).
Scenario C. Implicit in the above scenario B is the subdivision north and south of the Fortescue River valley. The Fortescue Valley is known to harbour a unique assemblage of invertebrate taxa (e.g. Durrant et al., 2010); however, there is potential for this substantial topographical discontinuity to act as a barrier to dispersal for small terrestrial vertebrates. In this case, we might expect to see stronger genetic divergence between taxa on either side of the central valley where there is a more pronounced topographical divide, whereas the flat and marshy headwaters in the east, and estuarine areas in the west, with their associated poorly defined channels, may facilitate movement of organisms into adjacent regions.
If local adaptation to distinct regions within the Pilbara, and the subsequent diversification of taxa within each region (scenarios A or B), or vicariance (scenario C) are responsible for the diversification of Pilbara biota, then taxa should exhibit phylogeographical structuring concordant with major geophysical and/or biophysical units. Furthermore, adaptation to distinct habitats should act to reduce gene flow between habitat types, resulting in greater genetic divergence between rather than within habitat types.
To assess the above predictions, we build on previous results with new and published molecular datasets to generate phylogenies for seven co-distributed gecko lineages. Specifically, we use this genetic information to address the following questions.
- Do taxa exhibit genetically differentiated populations across the Pilbara craton boundary?
- Within the Pilbara, is genetic diversity concordant with previously hypothesized regions (A, B or C, above), and is there congruence across taxa?
The timing of our study is significant. The Pilbara also has unique geological resources, endowed with rich deposits of minerals, oil and gas, and is the location for some of the world's largest mining operations for manganese and iron ore. The large-scale exploitation of these natural resources presents an ever-increasing challenge for conserving biodiversity in the region (Lloyd et al., 2002), and has been publicly acknowledged for short-range endemic invertebrate fauna in particular (Majer, 2009; Tomlinson & Boulton, 2010). With so little known of the distribution and partitioning of genetic diversity of low-vagility terrestrial vertebrates across the region, the potential for short-range endemism, particularly of habitat specialists, requires immediate attention.