A remarkable moment in Australian biogeography

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The evolution of Australia over the last 25 million years: the consequences of aridification and ice-age cycles. A special session of the Combined Australian Entomological Society's 36th AGM and Scientific Conference, 7th Invertebrate Biodiversity Conference, and Society of Australian Systematic Biologists and Conference. Australian National University, Canberra, Australia, December 2005

To borrow a Churchillian metaphor, Australian biogeography is a riddle wrapped in a mystery inside an enigma. There can be no doubt that a key driver of the evolution of the unique Australian biota was the development of quintessentially Australian dry and infertile landscapes. However, the rub is that there is vanishingly little specific information about when during the Cainozoic (Tertiary and Quaternary Periods), and how, the humid Gondwanic rainforests were transformed into the modern fire- and drought-adapted Australian biota. A recent meeting in Canberra entitled ‘The evolution of Australia over the last 25 million years: the consequences of aridification and ice-age cycles’ marks an important milestone in Australian biogeography. This meeting was facilitated by the Australian Research Council's Environmental Futures Network (http://nesuab.ees.adelaide.edu.au/page/default.asp?site=1). For the first time, researchers working on Australian palaeoecology and geomorphology and the relationships and phylogeography of plant, vertebrate and invertebrate groups were able to meet, compare data and recognize their remarkably convergent perspectives.

‘The lack of geological rejuvenation of the landscape, and attendant soil infertility, is thought to have been of critical importance in preadapting the Australian flora to aridity.’

Aridification during the Tertiary

Jim Bowler (University of Melbourne, Australia) and John Chappell (Australian National University (ANU), Canberra, Australia) provided sketches of the geomorphology of Australia emphasizing the progressive and intensifying aridification during the Tertiary. Humid landscapes with truly great lakes and rivers were transformed into arid lands with deeply weathered plateaux capped with laterite, desiccated river channels (palaeo-rivers), deflated lake beds and massive sandy and stony deserts. Bowler dramatically illustrated this by showing that the channel of the Murray River (which drains south-east Australia's largest catchment) currently meanders sinuously within its former riverbed – signifying a decline in river discharge by orders of magnitude. Chappell noted that the transportation of sand at the height of Quaternary aridity has buried landscape features to create a modern landscape with apparently isolated hills and ranges. Perhaps the most compelling evidence of late-Tertiary landscape aridification is the remarkable diversity and endemicity of a range of freshwater invertebrate groups now adapted to living in subterranean groundwater throughout inland Australia (known as stygofauna) (Leys et al., 2003). Steve Cooper (South Australian Museum (SAM), Adelaide, Australia) and Remko Leijs et al. (also from SAM) reported that molecular phylogenetic studies date the transition from surface to subterranean water by the stygofauna to about 5 million years ago (mya). Clearly, understanding Australian biogeographical patterns demands an understanding of the history of Tertiary geomorphology. In particular, many speakers, beginning with Bowler and including a number of biologists, recognized the period from 10 to 7 mya (Upper Pliocene–Lower Miocene) as critical to our understanding of the development of modern Australian ecosystems. This cooler, drier period (for which Bowler coined the term ‘Bob Hill discontinuity’) is sandwiched between a sequence of warm, humid environments in the early Miocene and late Pliocene. Importantly, this period is poorly represented in the fossil record, yet many arid-zone plant and animal lineages apparently date to this time window (Leys et al., 2003).

The lack of geological rejuvenation of the landscape, and attendant soil infertility, are thought to have been of critical importance in preadapting the Australian flora to aridity. Using the macrofossil record from south-eastern Australia, Bob Hill (University of Adelaide, Adelaide, Australia) traced systematic changes during the Tertiary to the abundance, distribution and protection of stomata in sclerophyll lineages such as Banksia, Callitris and Casuarina, which formerly occurred in rainforests. There have been dramatic changes in plant community composition throughout the Tertiary and into the first half of the Quaternary. David Bowman (Charles Darwin University, Darwin, Australia) posited that adaptation to fire, characteristic of the Australian flora, possibly originated from the monsoon tropics where ignition sources from lightning storms mark the transition from dry to wet seasons. Such a strongly seasonal climate, thought to have developed in the Tertiary, may have also preadapted taxa to aridification (Bowman & Prior, 2005). Bowman argued that the widespread landscape burning by late-Pleistocene human colonists was insignificant in the evolution of fire-adapted flora, but may have contributed to the extinction of megafauna by changing the vegetation structure. In this context, it must be acknowledged that the general lack of macrofossils of fire- (and drought)-adapted biomes is a serious impediment to understanding the evolution of Australian flora. However, the advent of molecular techniques to underpin phylogenetic and phylogeographical analyses has provided new insights into evolutionary processes and patterns of key groups (Crisp et al., 2004).

Using molecular techniques, Pauline Ladiges et al. (University of Melbourne) traced the radiation of eucalypts from ancestral and now relictual rainforest lineages thought to extend back to the early Cretaceous (Ladiges et al., 2003). They interpret the biogeographical distribution of modern eucalypts as reflecting basic splits in the lineage that preceded Tertiary aridity, thereby highlighting the great antiquity of the eucalypts. Likewise, Daniel Murphy et al. (Royal Botanic Gardens, Melbourne, Australia) presented DNA evidence for the antiquity of the species-rich and monophyletic Australian Acacia, which are almost entirely phylodenous. Murphy et al. found higher sequence variation in a relatively species-poor, arid-zone Acacia clade compared with a species-rich clade from the humid east coast (Fig. 1). They interpreted this as more recent radiation in the humid zone and compared with the more ancestral arid zone taxa.

Figure 1.

Cladogram of Australian Acacia (Acacia subgenus Phyllodineae), based on internal and external transcribed spacer nrDNA sequence data, showing the relative ages of four clades. Note bipinnate-leaved species are polyphyletic, with the eastern Australian Botrycephalae group being relatively younger than the Pulchelloidea clade. The Acacia victoriae clade from semiarid and arid regions of Australia is relatively old (an early node). (D.J. Murphy, P.Y. Ladiges and G.K. Brown, personal communication.)

Interactions

Perhaps the most compelling evidence for the antiquity of the modern drought-adapted flora concerns the radiation and diversification of gall-forming insects that parasitize trees by inducing the host to grow specialized structures to provide food, shelter and a stable microclimate (Fig. 2). It is probably no coincidence that Australia has the highest diversity of gall-forming insects in the world, given that galls are a superb adaptation to aridity (Gullan et al., 2005). Lyn Cook (ANU) and Penny Gullan (University of California, Davis, USA) reported the evolutionary congruence of molecular phylogenies between the highly diverse gall-forming scale insects with their equally diverse Myrtaceaous host tree species. Such parallel evolution is thought to reach deep into the Cainozoic, tracking the radiation and diversification of eucalypts. Michael McLeish (Flinders University, Adelaide, Australia) and Tom Chapman (also Flinders University) reported host specialization among gall thrips and arid-zone Acacia species. Their phylogenetic analysis suggests that the parallel evolution of gall thrips and Acacia occurred during the late Tertiary aridification. Sonja Scheffer et al. (US Department of Agriculture, Beltsville, MD, USA) reported the truly extraordinary case where Fergusinina flies and Fergusobia nematodes have coevolved a unique and obligate mutualism to parasitize myrtaceous trees. Fly oviposition occurs simultaneously with the deposition of juvenile nematodes, which induce gall formation on the host tree. The fly lavae and nematodes grow and feed inside the gall. When fully developed, nematodes enter the female fly larvae, where they remain until being deposited at the next oviposition site by the ensuing adult. In general, the flies and nematodes show host specificity for plant species from at least six genera (Eucalyptus, Melaleuca, Corymbia, Syzygium, Metrosideros and Angophora). Christine Lambkin (CSIRO Entomology, Canberra, Australia) and David Yeates et al. (CSIRO Entomology) reported on the timing of divergences in the species-rich, schlerophyll forest-fly family Therevidae, finding that the basic splits in the family predated Tertiary aridification, but that the major species-generating cladogenesis occurred during the most recent third of the Tertiary.

Figure 2.

Galls induced by females of Myrtaceae-feeding eriococcid scale insects in Australia. (a) Red galls of Eremococcus sp. on leaves of Agonis marginata. Male offspring develop within the maternal gall whereas females disperse. (b) Two galls of Apiomorpha malleeacola on a fruit of Eucalyptus socialis. Males induce separate, tube-shaped galls (not shown). (c) Three galls of Cystococcus pomiformis on Corymbia sp. These galls are commonly known as bloodwood apples or bush coconuts, and both the insect and the white flesh inside the gall are edible. Sons are produced first and develop within the maternal gall. When the males near maturity, daughters are produced. The tiny immature females climb onto the abdomen of adult males and are carried from the gall by their winged brothers. Photos (a,b) courtesy of Mike Crisp; (c) courtesy of Lyn Cook.

Physiologically, many Australian arid-zone mammals show the most extreme adaptations to aridification in comparison with other arid zones around the world. Ken Aplin (CSIRO Sustainable Ecosystems, Canberra) showed that many of the characteristic allochthonous arid-zone groups arose in the late Miocene and early Pliocene (at the time of the ‘Bob Hill discontinuity’), with novel adaptations to life in open (nonrainforest) habitats, and often without clear links to fossil lineages of earlier times. The marsupial mole is an exception, being of extremely old, isolated and endemic arid-zone specialist lineage.

Plant diversification

A recurrent feature of Australian phylogeography is strong local-to-regional-scale genetic diversification that appears to reflect a pattern of ‘cut-and-cut-again’ of existing populations (Fig. 1). This was well illustrated by Mike Crisp (ANU) and Lyn Cook, who explored the evolutionary effect of the Nullabor Plain that divides the south-eastern from the south-western temperate floras. They concluded that the numerous groups of allopatric sister taxa are the result of vicariant speciation associated with the formation of Nullabor biogeographical barrier(s) during the Tertiary, with divergences clustered in the period from 7 to 9 mya, and again at 2.5 mya. Margaret Byrne (Department of Conservation and Land Management (CALM), Perth, Australia) has found that three widespread trees species in south-western Western Australia, in different genera (Acacia, Eucalyptus and Santalum), all showed substantial and spatially congruent genetic (cpDNA) divergence. This phylogeographical pattern probably reflects past restriction to refugia during episodes of aridity during the Quaternary. Gay McKinnon et al. (University of Tasmania, Hobart, Australia) showed that the molecular phylogeography of Eucalyptus and Nothofagus in south-eastern Australia reflects the genetic impact of Pleistocene refugia. Paul Sunnucks's (Monash University, Melbourne, Australia) and Dave Rowell's (ANU) laboratories have focused on phylogeographical patterns in log-inhabiting, low-vagility invertebrates in a temperate, montane forest in south-eastern Australia. Their combined studies have shown remarkably high genetic divergences over very small distances, underlining the great stability of the forest habitats and microhabitat preferences of the organisms (Garrick et al., 2004). Phylogeographical patterns are consistent with repeated contraction into restricted refugia during the Quaternary glacial cycles of aridity. Sunnucks was led to generalize that ‘if it doesn't fly, it is a species complex’.

Teasing out phylogeographical patterns is highly problematic in most Australian environments because, unlike the atypical humid zone, there is an absence of reliable environmental archives such as pollen. Further, modelling palaeoclimates is difficult because of subdued topography and associated gentle rainfall and temperature gradients. Indeed, often the best evidence for environmental change is the phylogenetic patterns themselves. Given the inevitable reliance on molecular data, Craig Moritz's (University of California, Berkeley, USA) injunction to build phylogenies based on many, rather than single, genes is important and timely.

In sum, an emerging view from the meeting was that Australian ecosystems have been dramatically affected by increasing aridification on geological timescales right up to the present, and there was agreement concerning the great antiquity of the characteristically Australian plant and animal groups. This is reflected in deep divergences in molecular phylogenies, with many species lineages pushing well into the Pliocene; tightly coevolved mutualisms between plants and animals; many novel adaptations to escape the effects of aridification (stygobionts and gall-formers); and specific adaptations to soil infertility, drought stress and fire. The deepest divergences in characteristic arid-zone taxa often pre-date Tertiary aridification, suggesting biogeographical structuring in the mesic ecosystems of early Tertiary Australia. More recent phylogeographical patterns reflect numerous cycles of aridity throughout the Quaternary ice ages that created refugia and caused vicariant speciation or significant genetic differences among populations of widespread species.

The challenge for Australian biogeography is to move beyond these broad-brush generalizations by uncovering regional and continental phylogeographical patterns; assessing the phylogenic congruence among different taxa, particularly plants and animals; and integrating these data to make a coherent whole. To achieve this geological and biological knowledge, gaps must be filled. Fundamentally, the Tertiary fossil record for the northern and western half of the continent awaits discovery and documentation. A much better appreciation of the paleoclimates of the Late Miocene and earliest Pliocene (7–10 mya) is required because this period is emerging as critical in establishing the phylogenetic composition of the modern Australian biota. To help resolve inconsistencies between fossil and molecular chronologies, phylogeneticists need to refine methods of estimating divergence times. At the broadest scale, we need to move from phylogenies of individual lineages to phylogenies that encompass lineages characteristic of entire biomes, thereby bridging the gap between historical and ecological approaches to biogeography.

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