Ancient origins in Gondwana and evolution of the eucalypts in Australia
The origins and evolution of the eucalypts are strongly linked to the evolutionary history of the Australian continent, including the geological events associated with its origin and the environmental conditions that subsequently shaped the continent and forged its unique identify.
Evolutionary history of the continent
"The history of Australia as an individual entity is a post-Jurassic phenomenon" (Hill 1994, p. 2). This statement provides a clear reference point in the geological time-scale of about 135 million years BP for the origin and subsequent development of the present Australian continent. Australia's origin as a continent can be traced to its separation from other landmasses that made up the southern supercontinent of Gondwana. Other major Gondwana landmasses included Antarctica, South America, Africa, Madagascar, India and New Zealand. The subsequent development of the unique identity of the Australian continent took place during its drift northwards from far southern latitudes, over many thousands of kilometres and many millions of years, to its present location.
Continental separation and tectonics
The following summary of events associated with the separation of Australia from Antarctica and its subsequent drift into more northerly latitudes is derived from reviews by Quilty (1994) and Wilford and Brown (1994) and references therein. The reconstructions of these events must be viewed as conjectural at least to some extent, based as they are on limited evidence representing only relatively small sequences of the entire time course of events.
Separation of Australia from India and Antarctica is believed to have begun about 132 million years BP. The initial break-up took place in the north-west region of what is now the Australian continent and gradually extended southwards as Australia and India separated. This event was followed closely by Australia's separation from Antarctica from about 110 million years BP, beginning in the southwest and gradually extending east along the southern margins of the continent. The land connection between the two was eventually confined to the southern parts of Tasmania by about 80 million years BP. Final separation, followed by the formation of a deep marine strait between the two continents, had taken place by about 38 million years BP. Subsequently, the Australian Plate drifted slowly northwards, eventually colliding with the Pacific Plate and the Southeast Asian Plate. The northward drift of the Australian continent continues today.
The following summary of trends in Australian palaeoclimates has been based on reconstructions and information in reviews by Martin (1994), Quilty (1994) and Wilford and Brown (1994). Again it should be emphasised that relatively few data are available from which to infer geographical and temporal variation in climatic factors, particularly at the continent scale, but also over shorter time-scales. Therefore, reconstructions which infer trends in climate, particularly at these scales, remain largely conjectural.
Climatic conditions in Australia from about 140 million years BP are believed to have been cool and humid with some seasonality, at least for south-eastern parts of the continent, and with a gradient of increasing but still cool temperatures towards the northwest. Large parts of the continent were covered by sea during much of this period. By about 65 million years BP, conditions appear to have become much warmer and humid, and the seas had largely retreated from the continent. During the period 65 to about 45 million years BP, southern parts are thought to have experienced higher rainfall and temperate conditions, with warm temperatures in northern regions and a moisture gradient across the north of the continent which ranged from humid in the northwest to dry conditions in the northeast.
In contrast to the relative climatic stability of previous times, major variations in climate followed Australia's separation from Antarctica. This variability, which was characterised by marked fluctuations in temperature, rainfall, runoff and sea level, is thought to have resulted from the establishment of different marine and atmospheric circulation regimes as the Australian and Antarctic land masses moved further apart. A general cooling of sea temperatures in southern regions also occurred following separation of the continents, possibly associated with the development of a circumpolar oceanic flow. Antarctica is thought to have commenced its glacial phase at about this time with the development of sea ice. The cooling of Antarctica has been associated with increased temperature gradients between the polar region and the tropics, leading to increased wind strengths. Large-scale ice sheet development in East Antarctica from 38 to 36 million years BP is thought to have contributed to the onset of drier climates over much of Australia and the formation of wide-spread duricrusts (see Wilford and Brown, 1994).
From about 27 million years BP, temperatures appear to have become warmer across northern Australia, with tropical conditions evident at about the time of the collision of the Australian plate with the Southeast Asia plate. Modern circulation patterns for ocean and atmosphere appear to have become established as Australia moved closer to Asia and as the gap with Antarctica widened. In the period to about 18 million years BP, there is evidence for humid conditions in central Australia with substantial lake systems, watercourses and dense vegetation. In contrast, subsequent periods have been associated with a change to more seasonal conditions with marked dry periods. Fire is thought to have become an important element in the Australian environment at about this time (Martin 1989).
Climates during the Late Tertiary (10 to 2.2 million years BP) and the Quaternary (2.2 million years BP to present) are believed to have become increasingly variable, and there is evidence to suggest a gradual drying out of the continent (see Bowler 1982). A warm, wetter phase occurred in southern Australia in the period after about 10 million years BP. There is also evidence for a warmer period in Antarctica at about this time (see Quilty 1994). This phase was followed by a gradual return to drier conditions in Australia, which is thought to have been associated with the transition from rainforest to wet sclerophyll vegetation and eventually to more open vegetation types, including grasslands. There is evidence that relatively rapid alternations between rainforest and sclerophyllous vegetation occurred at some places (Truswell 1990). Sea temperatures to the south of Australia continued to decline during this period and Antarctica entered its present glacial phase at about 2.6 to 2.4 million years BP. Conditions in southern and central parts of the Australian continent became more arid at about this time, with tropical conditions persisting in the north.
The present pattern of polar glaciation became established during this most recent period, with at least 17 glacial periods documented as occurring during the past 2 million years BP. Each glacial cycle has been associated with a prolonged period of increasing icecap volume at the poles and decreasing sealevel, followed by a short-term collapse of the icecap and a sudden increase in sealevel. Although the chronologies of earlier glacial cycles are poorly known, the most recent seem to have involved a glacial period of about 100,000 years, a collapse period of about 10,000 years, and a stable, interglacial period of between 5,000 and 10,000 years. The glacial periods are believed to have been associated with cold, dry and windy conditions on the Australian continent, leading to a large expansion of the continental arid zone, reduced incidence of tropical cyclones in the north, and increased snowfall with some glaciation at higher elevations. Stable interglacial periods, which includes the present time, are generally associated with warmer and less arid conditions.
The following summary of Australian landscapes has been derived largely from a recent review by Taylor (1994). The landscapes of Australia are predominantly ancient, although younger formations occur in some parts. In general, the western two thirds of the continent is dominated by older landscapes of lower relief and the eastern third includes younger and higher relief landscapes, particularly associated with the Eastern Highlands. Australia’s ancient landscapes include some that are considerably older than the breakup of Gondwana, including examples dating back as far as Precambrian times (prior to 570 million years BP).
Much of the Australian continent is dominated by landscapes of low relief. Many of these comprise younger sedimentary basins partly overlying much older rocks. The Eastern Highlands include older rocks superimposed by younger landscapes, such as those formed by basalt flows. With some exceptions, basalt landscapes along the eastern margins of the continent exhibit a general north-south trend of decreasing age, ranging from Late Cretaceous (before 65 million years BP) in the north, to Holocene (10,000 years BP to present) in the south. Marine inundation has also affected parts of the continent at different times. Many of the higher elevation areas are thought to have been separated by shallow seaways at these times, which is likely to have contributed to increased spatial and habitat diversity (Wasson 1982).
The land surfaces of a large part of the continent comprise a regolith (ie material overlying bedrock) of either sedimentary deposits derived from weathering or erosion of older surfaces, or deeply weathered in situ material derived from the underlying parent rocks. These ancient landscapes have undergone deep weathering and soil formation over very long periods associated with Australia's exceptionally stable tectonic conditions.
The soils of the majority of Australian landscapes are characteristically highly-leached and infertile. Humid periods from the Cretaceous to the Pliocene are believed to have contributed to widespread deep weathering and the formation of leached acid soils of low nutrient status that are characteristic of large parts of the continent. Drier conditions in the Quaternary led to a change in weathering processes and the formation of the alkaline soils with a high salt or carbonate content that are widespread throughout the drier parts of central and southern Australia.
Tertiary and Quaternary phytogeography
The following overview of phytogeography in Australia during the Tertiary (65 to 2.2 million years BP) and Quaternary (2.2 million years BP to present) has been drawn largely from recent reviews by Martin (1994), Kershaw et al. (1994), Macphail et al. (1994) and Hope (1994). Their reconstructions of the phytogeography of the Australian continent during these periods have been based on the fossil pollen record. It should be noted that generalisations that form the basis of these reconstructions neither encompass the actual spatial diversity of vegetation that may be present in the landscape nor deal comprehensively with its temporal variation. As Martin (1994) points out, reconstructions relate to the dominant types of vegetation in the landscape and they largely exclude small areas of different types of vegetation.
In general, the spatial variation exhibited by past vegetation in Australia is thought likely to have been comparable with the present-day vegetation (Martin 1994). All the fossil evidence shows that the flora was not uniform at any time (Martin 1994). In this regard, Macphail et al. (1994) also commented that "there is no compelling evidence for a pan-Australian flora ...". Temporal change in the vegetation was also likely to have been ongoing and gradual, with occasional periods of drastic change, probably associated with times of major climate change (Martin 1994).
The Australian landscape was largely forested throughout the Tertiary (Martin 1994). Palaeocene (65 to 54 million years BP) vegetation in southeast Australia is believed to have been dominated by coniferous wet forests that were able to withstand the long, dark winters of southern latitudes (Macphail et al. 1994). A gradient from wetter coastal areas to drier inland areas is thought to have persisted across the continent for much of this period (Martin 1994, Kershaw et al. 1994). Inland areas were probably dominated by rainforest-type vegetation with angiosperm dominants. Little is known of the vegetation of northern and western Australia at this time.
The conifer-dominated rainforest of southeast Australia appears to have been replaced by angiosperm-dominated rainforest during the Eocene (54 to 38 million years BP. Rainforest with Nothofagus species is thought to have become a dominant vegetation type during the Late Eocene, at least for southern parts of the continent (Martin 1994), and was possibly associated with a phase of global cooling (Macphail et al. 1994). There is some evidence of eucalypt-dominated vegetation in the Early to Middle Miocene, but its distribution appears to have been limited and there is little evidence of grassland and open sclerophyllous vegetation (Kershaw et al. 1994).
Mid to Late Miocene vegetation has been associated with the disappearance of Nothofagus from many areas and an increase in Myrtaceae, but with some rainforest taxa still present. It has been suggested that the vegetation at this time may have been predominantly wet sclerophyll, perhaps with a rainforest understorey (Martin 1994). Macphail et al. (1994) have also suggested there was a marked contrast between coastal and inland environments.
An increase in charcoal content in the fossil record occurred during the Miocene, possibly reflecting a change to an increased incidence of fires (Kershaw et al. 1994, Martin 1994). Kershaw et al. (1994) also discussed the possibility that increasing temperatures in the Mid Miocene associated with an effective reduction in precipitation may have contributed to this change in fire regime. A paucity of pollen evidence from the very Late Miocene is also consistent with drier or to more variable climatic conditions (Kershaw et al. 1994).
Rainforest vegetation increased again in the Early Pliocene, although the spatial incidence of this was extremely variable, which may reflect vegetation mosaics of rainforest in wetter habitats and wet sclerophyll in drier habitats. By the Mid to Late Pliocene a dominant Myrtaceae component of the vegetation was again evident.
The Late Pliocene to Pleistocene record demonstrates further substantial vegetation change, particularly associated with an increasing component of herbs and grasses. The increased herbaceous component is believed to reflect a transition towards vegetation with a more open structure, such as woodland and grassland (see Martin 1994). This change is first evident in the northwest of the continent, extending later to southern regions (Kershaw et al. 1994). There is little evidence for the presence of open-canopied vegetation in the period prior to the Miocene, suggesting this vegetation type was either absent or very restricted (Kershaw et al. 1994).
The present-day vegetation types that occur in Australia are believed to have developed by the end of the Pliocene (Kershaw et al. 1994), although marked changes in their distribution and relative contribution to the flora would have occurred as a result of the climate changes of the Pleistocene and Holocene periods.
In summary, major changes in Australia's vegetation occurred during the Tertiary and Quaternary which involved a transition from coniferous and rainforest dominated vegetation to a predominantly open-sclerophyll vegetation with rainforest confined to wetter localities. As part of this transition, eucalypt-dominated vegetation expanded greatly in distribution at the expense of other vegetation types, including the drier rainforests, Casuarinaceae-dominated forests, and wet sclerophyll forests with non-eucalypt dominants from the family Myrtaceae. These changes were also associated with an increased grassy understorey component in more open eucalypt-dominated communities and the development of temperate grasslands in some areas (see Kershaw et al. 1994). Factors thought to have been important in influencing these changes to the vegetation include increased climatic variability, a transition to drier climatic conditions, the effects of the extreme glacial/interglacial cycles of the past 2 million years, and an increased incidence of fires. The latter may also have been influenced in more recent times by the arrival of humans on the continent.
Evolution of the eucalypts
The fossil record
The fossil record of the eucalypts, including both macrofossils and pollen, is poor with relatively few specimens that have been reliably identified and dated (Hill 1994). The earliest records of eucalypt-type pollen in Australia are of Late Paleocene age (to 54 million years BP) (see Martin 1994). Pollen types with close affinities to extant eucalypt taxa first appear in the Late Oligocene (to 27 million years BP). For example, pollen with close affinities to the extant species Eucalyptus spathulata has been identified at sites of Pliocene age (10 to 2.2 million years BP) from both the southeast and southwest of the continent (Martin and Gadek 1988); in the southeast, this fossil pollen type extends well into the Pleistocene (after 2.2 million years BP). The more recent pollen record tends to exhibit a greatly increased abundance of eucalypt pollen compared with previous periods (see Martin 1994). This is often associated with increased amounts of charcoal. It has been suggested that the increased charcoal may reflect an increased incidence of fires, perhaps associated with a drying climate (Hill 1994), and also with the influence of humans (Singh et al. 1981, Kershaw 1986).
Reliably-dated eucalypt macrofossils are mostly from the south-east of the continent. Well-preserved eucalypt-like fossils have been found in central Australia (e.g. Lange 1978), but their age is uncertain (Ambrose et al. 1979). The oldest accurately-dated eucalypt macrofossil is estimated as 21 million years BP (Bishop and Bamber 1985). Other reliably-identified eucalypt fossils, including fruits and leaves comparable to extant taxa, have been dated from the Middle Miocene (17 to 14 million years BP) (e.g. Holmes et al. 1982), and the Pliocene (10 to 2.2 million years BP) (e.g. Pole et al. 1993). Fossil flower remnants of Late Miocene age (10 to 5 million years BP) represent the earliest evidence of the eucalypt subgenus Monocalyptus; these deposits also include specimens associated with the subgenus Symphyomyrtus (Blazey 1994).
Macrofossils with affinities to the eucalypts have also been reported from other countries which have no extant eucalypts in their natural floras. These extra-Australian records include fossilised fruits and leaves of Early Miocene age from New Zealand (Pole 1989, 1993) and fossilised fruits from sediments of Miocene age in Patagonia on the South American continent (Frenguelli 1953). In addition, fossilised leaf material with affinities to the eucalypts has been collected more recently in Patagonia by Romero (see Hill 1994). The New Zealand fossils have been described by Hill (1994) as more reliable that those from South America, although Ladiges (1997) notes that without definitive characters none of this material can be reliably attributed to Angophora or Eucalyptus. Hill (1994) also draws attention to the records of eucalypt-type pollen in New Zealand, listed by Mildenhall (1980) as having a stratigraphic age of Miocene to Early Pliocene.
Extant eucalypt species are nearly all endemic (confined in their natural distribution) to the Australian continent. Exceptions include four species that occur in tropical parts of Asia, but are not found in Australia. These are Eucalyptus deglupta which is endemic to parts of Indonesia, northern New Guinea, New Britain and the southern Philippines, and E. urophylla, E. orophyla and E. wetarensis which occur in Timor and the nearby Lesser Sunda islands (Pryor et al. 1995). A further ten species are common to Irian Jaya and Papua New Guinea and areas of northern Australia (Eldridge et al. 1993).
The closest living relatives of the eucalypts include the genera Arillastrum which is endemic to New Caledonia, Eucalyptopsis which occurs in northern Australia and New Guinea, and Allosyncarpia and Stockwellia, both of which occur in northern Australia.
Origin of the eucalypts
The palynological record for the family Myrtaceae, to which the eucalypts belong, indicates a Late Cretaceous distribution that included Borneo (90 to 85 million years BP), Africa (85 to 80 million years BP), South America (70 to 65 million years BP) and Antarctica (80 to 65 million years BP). The Antarctic records are earlier than the first records for the Myrtaceae in Australia and New Zealand (65 to 54 million years BP).
As mentioned above, the earliest records for eucalypt-like pollen in Australia date from about 54 million years BP, and the earliest fossil evidence of pollen with strong affinities to extant eucalypt species occurred about 27 million years BP. The palynological evidence therefore supports the presence of eucalypts in Australia and New Zealand during at least the early Tertiary.
The available macrofossil evidence raises the possibility that there may have been eucalypts in New Zealand and South America during the middle of the Tertiary. Hill (1994) and Ladiges (1997) discuss hypotheses to explain these more remote, though unconfirmed records, in terms of the origins and distribution of the eucalypts. Two hypotheses have been proposed, viz: either the fossils represent an ancient lineage for the eucalypts which was more widely distributed in Gondwana prior to the break-up or, alternatively, the fossils resulted from long-distance dispersal either from Australia or from some other part of the natural distribution of the eucalypts. Either hypothesis might explain the New Zealand fossils, whereas verification of the South American fossils as eucalypts would constitute stronger support for the former explanation. There is no clear fossil evidence to support either of these explanations to date.
In considering the biogeographic evidence, it is important to note that Angophora, Corymbia and Eucalyptussensu stricto are most closely related to Arillastrum, which is endemic to New Caledonia. The split between these two groups may therefore be as old as the split of New Caledonia from the Australian land mass, which formed part of Gondwana. This evidence suggests the eucalypts may date back at least to the Late Cretaceous (about 80 million years BP), which is older than the fossil record indicates (Ladiges 1997, Ladiges pers. comm. 1999).
Although the actual origins of the eucalypts remain uncertain, it is clear that Myrtaceous taxa, which may have included eucalypt precursors, were present in the landmasses that comprised Gondwana prior to its breakup. It is also clear that the eucalypts have been present on the Australian continent since the early Tertiary, prior to its final separation from Antarctica. The natural distribution of extant eucalypt taxa, which are almost all confined to the Australian continent and with only very few taxa occurring naturally in other, nearby parts of the world, is consistent with either a Gondwanan or Australian origin for the eucalypts. In this regard, Barlow (1981) referred to evidence in Gill (1975) and Martin (1981) when he commented "For phytogeographical reasons alone there can be little doubt that Eucalyptus is of ancient Australian origin, although the genus does not appear definitely in the fossil record until the Oligocene” (p. 58).
The following discussion of the evolution of the eucalypts builds on the few factual data available concerning historical distributions of the eucalypts, and also draws upon the reconstructions of past geological events, landscapes, palaeoclimates and vegetation discussed in previous sections. There is little direct evidence available as yet from which the evolution of the eucalypts can be reconstructed with any degree of certainty.
Within the context of reconstructed changes in Australian environments and vegetation, it seems that the eucalypts or their ancestral forms persisted and evolved through the transition from the relatively predictable moist climates and closed vegetation that characterise the early Tertiary, to the highly variable and drier climates and more open vegetation of the late Tertiary and the Quaternary.
Lange (1980) proposed that the vegetation of the Mid Tertiary may have comprised predominantly wetter non-eucalypt vegetation around the margins of the continent and drier vegetation with eucalypts in central regions. Under this scenario, the transition to drier climates may have ultimately resulted in displacement of the eucalypts to the continental margins, and restriction of non-eucalypt vegetation to the wettest areas and its loss altogether from parts of the continent. Hill (1994) commented that the available fossil evidence is not inconsistent with this hypothesis.
The most-recently-evolved component of the Australian flora is called the "autochthonous" element and is readily distinguished from the ancient "Gondwanan" or "relict" and the recently-invaded "tropical" elements of the flora (see Burbidge 1960, Barlow 1981, Martin 1994, Wardell-Johnson et al. 1997). Barlow (1981) described the autochthonous element as comprising "those elements of the flora which have undergone considerable evolutionary change, under conditions of geographical isolation, to produce typically Australian taxa with high levels of endemism" (p. 44). The eucalypts comprise an important part of the autochthonous element of the flora (Martin 1994).
Scleromorphy has been described as one of the more striking aspects of the autochthonous flora (Barlow 1981). Scleromorphs, as the name suggests, have hard, stiff leaves that are heavily cutinized (called sclerophylly). Sclerophyllous vegetation typically comprises woody plants with hard, tough and generally smaller leaves and is characteristic of dry places (see Usher 1979), particularly of Mediterranean-type climates. It has also been interpreted as a response to low nutrient soils (e.g. Beadle 1966). Scleromorphy is strongly represented in Australia by a number of plant families including Myrtaceae, Proteaceae, Rutaceae, Epacridaceae, Mimosaceae, Fabaceae, Goodeniaceae and Casuarinaceae (Barlow 1994).
It has been proposed that the scleromorphic element of the Australian flora, which includes the eucalypts, may have originated on the margins of areas dominated by rainforest, perhaps as an adaptation to low soil fertility (see Andrews 1913, 1916, Beadle 1981). Specht's (1981) observation, that sclerophyllous heath communities are part of Australia's moist tropical ecosystems today, where they form a mosaic with closed forest communities in response to deep, infertile, sandy soils, is consistent with this view. If the above hypothesis is correct, the characteristics of the eucalypts may have constituted a pre-adaptation rather than a direct adaptation to environmental factors favouring scleromorphic vegetation, such as increasing aridity or an increased incidence of fires (see Barlow 1981).
Johnson and Briggs (1981) similarly proposed that scleromorphy in Australia may have evolved in the early Tertiary on nutrient-deficient forest sites. Radiation of scleromorphic taxa would have occurred as the soils of large parts of the continent became impoverished and the climate became drier. The pollen record is generally consistent with this view, showing progressive transitions from rainforest to wet sclerophyll forest to dry sclerophyll vegetation followed by a relatively sudden transition to open sclerophyll vegetation during the period from the Mid Miocene (17 million years BP) to the Late Pliocene/Pleistocene (about 2.2 million years BP) (Martin 1994).
The high degree of adaptation by species to the presence of fires, through different fire regimes, amongst the sclerophyllous element may also be indicative that fire has been an important factor in the evolution of this component of the Australian flora. The charcoal record in pollen cores supports the hypothesis that fire was present in Australian environments throughout the Tertiary, and that its activity increased in association with the changes towards drier climates and increased seasonality of rainfall that occurred subsequently (Kershaw et al. 1994).
Hill (1994) noted both that there has been a dramatic increase in abundance of eucalypt pollen in recent sediments and that has this occurred in association with increased charcoal levels. This has been interpreted as consistent with the geographic expansion of the eucalypts to dominate the continent (see Hill 1994). The possibility that Aborigines may have played a role in increasing the incidence of fires and therefore in promoting the current dominance of the vegetation by the eucalypts has also been raised (e.g. Singh et al. 1981, Kershaw 1986). In this regard, Martin (1994) noted that rainforest vegetation requires exceptionally dry conditions to burn and that Aboriginal burning by itself would be insufficient to cause a widespread decline of rainforest. Drier climates are also likely to have contributed to the recent expansion of the eucalypts due to an increased incidence of fires (Hill 1994). The changing temperature and rainfall patterns associated with the glacial cycles over the past 2 million years would also have had pronounced effects on eucalypt distribution.
Outstanding universal value: Ancient origins in Gondwana and evolution in Australia
The eucalypts have outstanding universal value as an ancient, monophyletic lineage that has evolved and persisted on the Australian continent and nearby islands and is now unique to these areas. The origins of the eucalypts were on landmasses that formed part of the supercontinent of Gondwana, and their evolution took place subsequent to its breakup and the separation of these landmasses.
The evolution of the eucalypts is intimately linked to the Australian continent, having been influenced by its ancient, flat landscapes of unusual tectonic stability, its heavily-leached, nutrient-poor soils, and also by the environmental changes that resulted during the northwards drift of the continent to reach its present position. These environmental changes included a broad transition from a wet, stable climate at higher latitudes to a variable but drier climate with increasing periods of aridity at lower latitudes. The drier periods may also have been associated with increased incidence of fire in some areas. While maintaining a general drying trend, these climatic changes appear to have oscillated to some extent between wetter and drier climates at different times.
At the broadest scale, these past changes in environmental conditions have been associated with a transition of the dominant vegetation types of the continent from conifer-dominated rainforest to angiosperm-dominated rainforest, to wet sclerophyll forest, and then to progressively more open sclerophyll forest and woodland with an increasing grassy component. The eucalypts are believed to have originated on the margins of rainforest patches, and to have evolved in response to low nutrient soils that were seldom waterlogged, a drying climate and an increased incidence of fires.
The pollen record shows that the eucalypts have played an increasingly prominent role in the vegetation, often dominating the sclerophyll vegetation types as they increased in distribution, and eventually expanding to dominate almost all of the woody vegetation of the entire continent. The eucalypts are therefore one of the most important components of the recently-evolved, or autochthonous, element of the Australian flora. Their evolution has paralleled that of the continent, and their particular adaptations and characteristics reflect this history as well as contributing in a major way to the unique character of Australia's present environments and vegetation.
Current understanding of evolutionary relationships and ongoing evolutionary processes
A recent review by Ladiges (1997) provides a summary of current understanding of evolutionary relationships amongst the eucalypts based on morphological and molecular studies. As discussed previously, the evidence that the eucalypts represent a monophyletic lineage is strong (see eucalypt phylogeny section above). Moreover, within this single lineage, it is also clear that there are a number of eucalypt groups which have been classified as genera, or informally as sub-genera, based on morphological evidence.
Recent molecular evidence based on DNA data (Udovicic et al. 1995) shows two major evolutionary lineages (branches or clades) amongst eucalypt taxa currently in the genera Angophora and Eucalyptus sensu lato (including the bloodwoods). One clade comprises Angophora and the bloodwood sub-genera Corymbia and Blakella, and the other includes the remaining subgenera within Eucalyptus sensu stricto. A summary tree of phylogenetic relationships of the major groups of eucalypts, based on both morphological and molecular data, has been published (see Ladiges 1997, Figure 2.2, p. 20) and characters diagnostic to these eucalypt groups listed (Ladiges 1997, pp 18-22 and Table 2.1). The analyses also indicate that some of the morphological features used in previous taxonomic classifications of Eucalyptus have evolved more than once.
The Angophora lineage shows a further division into two branches, corresponding with Angophora and the bloodwoods. Three lineages are evident amongst the non-bloodwood eucalypts included in Eucalyptussensu stricto; these include an older lineage comprising the sub-genus Eudesmia (20 species) and two others represented by the large sub-genera Symphyomyrtus (>300 species) and Monocalyptus (>120 species) (see Ladiges 1997, Figure 2.2). Basal taxa associated with the Symphyomyrtus and Monocalyptus lineages have been identified. The species Eucalyptus guilfoylei and E. microcorys are basal both to Symphyomyrtus and to the closely-related sub-genus Telocalyptus. Taxa basal to the Monocalyptus lineage include Eucalyptus curtisii, E. tenuipes, E. cloeziana and E. rubiginosa (Ladiges 1997, P. Ladiges personal communication).
The major eucalypt groups differ in their biogeographic distributions within Australia, and these differences may be relevant to understanding evolutionary relationships amongst the eucalypts as well as inferring historical distributions and interpreting the implications of physiological constraints and tolerances. Overviews of the distributions of the major eucalypt groups may be found in Gill et al. (1985) and Ladiges (1997). A brief summary of these distributions follows.
Taxa of the Angophora-bloodwood group occur widely in tropical, sub-tropical and warm-temperate regions of the continent but are not found in the cooler southern regions (Ladiges 1997). The major concentration of the bloodwoods is in the northern, tropical savannah regions (Gill et al. 1985). Some taxa in Corymbia extend into southern areas, with particular species exclusive either to the east or the west of the continent. Ladiges (1997) noted that this east-west division may be evidence for an older lineage that pre-dates the ancient biogeographic isolation of the two parts of the continent or, alternatively, it may reflect more recent long-distance dispersal.
The Telocalyptus group occurs only in northern latitudes. This group, which is closely related to Symphyomyrtus, includes one species confined to the northwest of Australia, and two species restricted to the northeast. In addition, there is a fourth species, E. deglupta, which is endemic to New Guinea, New Britain, Ceram, Sulawesi and Mindinao in the southern Philippines, and probably reflects an early dispersal event from Australia or New Guinea perhaps associated with tectonic events (see Ladiges 1997).
The Symphyomyrtus group is the most widespread of the eucalypts as it occurs throughout the Australian continent, including the drier areas, and also has taxa common to northern Australia, Indonesia and New Guinea. Within the Symphyomyrtus lineage, the oldest, basal taxa also show an east-west division, with E guilfoylei (yellow tingle) occurring in the southwest and E. microcorys (tallowwood) in the east of the continent (Ladiges 1997).
The Monocalyptus group shows a predominantly southern distribution, extending also up the east coast. It also includes taxa confined to either the west or the east of the continent (Gill et al. 1985). The oldest basal taxa within the Monocalyptus lineage, including E. curtisii, E. tenuipes, E. cloeziana and E. rubiginosa are all found in the northeast of Australia. Interestingly, these basal taxa or “living fossils” also occur together with representatives of all the other sub-genera at Isla Gorge in southeast Queensland. Ladiges (1997) noted that this unusual combination is suggestive of relictual taxa (only remaining species of particular lineages) and an early biogeographic separation of northern areas from southern parts of the continent.
A recent review of patterns of eucalypt genetics and breeding systems provides an overview of mechanisms for promoting gene flow and genetic mixing amongst eucalypts (see Potts and Wiltshire 1997). These mechanisms include divergence, hybridization and introgression and the establishment of reproductive barriers between small populations (Potts and Wiltshire 1997).
The observed patterns of biogeographic distribution for eucalypts are generally consistent with a model of evolutionary divergence based on a combination of differentiation along ecological gradients and speciation in geographical isolation (allopatric speciation) (see Ladiges 1997). Closely-related eucalypt species tend to display patterns of spatial separation from each other which may be the effect of processes of variation and adaptation to environmental change, culminating in genetic divergence and speciation. The observed partitioning of closely-related species along major environmental gradients, such as climate, topography, and soils, is consistent with this model (Austin et al. 1997). Marked genetic variation reflecting adaptation divergence along steep environmental gradients has been demonstrated amongst co-occurring taxa over relatively short distances and within continuous stands. Morphological and physiological studies also suggest close adaptation of populations to local conditions for many characters (see Potts and Wiltshire 1997). Adaptive changes in response to habitat factors may also lead to genetic divergence within a species and ultimately to speciation.
Broader patterns of spatial separation between related taxa may reflect geographical isolation, leading to divergence and speciation. Patterns of genetic diversity between populations of some eucalypt species are consistent with this interpretation. For example, a high proportion of the observed genetic variation for widespread species such as E. delegatensis and E. nitens has been shown to correspond to major geographic disjunctions within their range (Moran 1992).
Hybridisation is an active and ongoing process amongst potentially-interbreeding eucalypt species which increases genetic variability and thereby facilitates adaptive change. Some eucalypt species are able to hybridize where they come into contact, although other species are genetically isolated. The frequency of natural hybrid combinations tends to decrease with increasing taxonomic distance (Griffin et al. 1988). Genetic isolation is also characteristic of higher taxonomic levels amongst the eucalypts. A possible exception is the recorded hybridization between species of two closely related subgenera Idiogenes (E. cloeziana) and Monocalyptus (E. acmenoides) (Brooker and Kleinig 1994), although recent DNA analyses have raised concerns about the subgeneric classifications of the species involved (see Potts and Wiltshire 1997).
Natural hybrids tend to occur at habitat boundaries between parent species. Where these boundaries are sharp, hybrids may be absent, or occur as isolated individuals; where the boundaries are gradual, many hybrids may occur in a "hybrid swarm", sometimes including progeny beyond the first hybrid generation. Hybrid swarms that persist and become geographically isolated from one or both of their parent taxa are known as "phantom hybrids" (see Pryor and Johnson 1971, Potts and Wiltshire 1997).
Hybrids may also occur as zones of introgression (see Potts and Wiltshire 1997). Introgression is the introduction of genes from one species into the population of a closely-related species during hybridization. In this case, hybridization may provide a mechanism for adaptive or neutral gene flow to occur. Introgression may also result in resurrection and dominance of the phenotype of the pollen parent.
Hybridisation has the potential to increase genetic variability amongst eucalypts, but there may also be a subsequent loss of this increased genetic variability from a population; for example, as a result of reduced vigour, fitness or reproductive capacity in hybrid progeny compared with parent types (see Ladiges 1997, Potts and Wiltshire 1997, Wardell-Johnson et al. 1997).
Reproductive barriers to prevent hybridisation and inhibit gene flow are found in natural eucalypt populations. These barriers are important in maintaining genetic integrity of populations, and may play a major role in the survival of rare or relict species. Reproductive barriers in eucalypts include spatial separation of potentially-interbreeding populations, and temporal separation involving different flowering times for species. The use of different pollinators by different species may constitute a reproductive barrier, although this has yet to be investigated. Structural and physiological barriers which interfere with fertilization processes also occur in some species (see Potts and Wiltshire 1997 and references therein).
Divergence, hybridization and introgression are active processes that are ongoing amongst the eucalypts. Although there is no definitive evidence that ongoing speciation is occurring amongst the eucalypts at the present time, these mechanisms may be of major importance in contributing to the wide genetic variation observed amongst eucalypt populations and species.
The overall level of genetic diversity of the eucalypts is high (Moran 1992). Similar high levels of genetic diversity are common among many widespread tree species (see Potts and Wiltshire 1997). The average percentage of genetic diversity between populations for eucalypts has been estimated at more than twice the average diversity for both wind-pollinated conifers and wind-pollinated angiosperms in the northern hemisphere (Moran 1992). This difference appears to be consistent with taxa that have animal pollination and poor seed dispersal and which show increased genetic differentiation between populations (see Potts and Wiltshire 1997). Eucalypts also exhibit high levels of genetic diversity within populations, comparable with gymnosperms and other long-lived woody perennials (see Potts and Wiltshire 1997).
The eucalypts themselves vary widely in terms of overall levels and distribution of genetic diversity. Widespread eucalypt species tend to have greater levels of between- and within-population genetic diversity compared with more localised species (Potts and Wiltshire 1997). Genetic diversity between populations tends to be higher in species with disjunct distributions compared with those with continuous distributions. This may be due to increased genetic differentiation in populations which are smaller and have been isolated over long time periods (Moran 1992). Populations of some rare species have also been shown to be genetically depauperate (see Crisp 1988, Potts and Wiltshire 1997). The relationship between genetic diversity within eucalypt populations and population size is not clear, with some studies showing a correlation, but others showing no relationship (see Potts and Wiltshire 1997). There is also no indication that populations that are outliers in the distribution of eucalypt species have reduced genetic diversity compared with those located centrally.
Contribution to outstanding universal value: Evolutionary relationships and processes
The evolution of the eucalypts in Australia is reflected in the phylogenetic relationships among and within the main eucalypt groups. These groups appear to reflect ancient branches of the eucalypt family tree and they are central to the story of the evolution of the eucalypts on the Australian continent, contributing to its outstanding universal value.
The current biogeographic distributions of the main eucalypt groups are also important in shedding light on aspects of the evolution and historical biogeography of the eucalypts. The larger of these groups have predominantly northern, southern or widespread distributions, probably resulting from different evolutionary pathways and historical constraints.
Sites of co-occurrence of the main groups and also of particular taxa that are basal on the main branches of the evolutionary tree of the eucalypts are likely to represent important, relictual sites associated with ancient biogeographic distributions. The restriction of certain taxa to the west or to the east in the southern parts of the continent is also thought to be important in representing aspects of past biogeographic distributions of the eucalypts. These and other disjunct aspects of distribution may also be important in reflecting the impact of changes in climate and environmental conditions resulting in long-term isolation of taxa in different parts of the continent and their subsequent evolutionary divergence to form distinctive components of the present-day flora.
The eucalypts have a high level of genetic diversity and also exhibit a range of active processes for increasing genetic diversity, including divergence, hybridisation and introgression. These processes may be important in the continuing evolution of the eucalypts, although there is, as yet, no definitive evidence that speciation is occurring under present-day conditions.
Eucalypts have been described as globally outstanding in an evolutionary context in relation to their wide and rapid radiation, adaptation, and hybridisation (Costin 1989, p. 16). It is likely that the high levels of genetic diversity of the eucalypts have been crucial in their evolutionary diversification and the success of their geographic expansion to dominate a wide range of environments across the entire continent.
Taxonomic diversity of the eucalypts
The eucalypts are highly diversified (Pryor and Johnson 1971), currently including more than 700 species (Brooker and Kleinig 1994). The species are distributed amongst the major eucalypt groups as follows: Angophora (11-13 species); Corymbia gen.nov (102+ species) and Eucalyptussensu stricto (600 species) (see Ladiges 1997, Table 2.1, pp. 18-19). All but four of these species occur in Australia.
Although the overall taxonomic differentiation amongst the eucalypts is very high, there are other taxa world-wide of dominant woody genera with similar or higher levels of taxonomic diversity. Amongst these other large genera of dominant woody species, Acacia has an estimated 1200 species world-wide, including about 900 species in Australia, Ficus includes 750 species (although not all of these are either dominant or woody species), Quercus has 400 species, Salix includes 400 species, Shorea includes 357 species, Dipterocarpus includes 69 species, and Pinus has 93 species (Mabberley 1997).
An unusual feature of the eucalypts is related to the fact that they represent a large taxonomic group of woody dominants which has diverged almost entirely on a single continent. Although Acacia is more taxonomically diverse than the eucalypts and also has more species within Australia, particularly including the phyllodinous species (those with leaves reduced to expanded petioles, or phyllodes), the genus has a much wider distribution globally than the eucalypts. With the possible exception of Dipterocarpus, other taxonomically-diverse dominant woody genera also tend to have much wider distributions globally (see Mabberley 1997).
The Australian autochthonous flora has been described as "predominantly temperate and arid-adapted, showing massive evolutionary diversification from the more labile of the ancestral Gondwanan stocks and characterised by scleromorphy and high endemism" (Barlow 1981, p. 44). The eucalypts are an exemplar of these aspects of the autochthonous flora, exhibiting very high levels of evolutionary diversification, development of scleromorphy and high levels of regional endemism within the Australian continent. Their extraordinary taxonomic diversity has resulted from this “massive” evolutionary diversification (Barlow 1981).
Eucalypt-dominated vegetation exhibits relatively high levels of diversity of eucalypt species. In general, the richness of eucalypt species within particular community samples, called within-habitat or "alpha" diversity (see Whittaker 1975), is variable and often low. The alpha diversity of eucalypts depends strongly on habitat type. In contrast, the degree of change in species composition of eucalypts along an environmental gradient, called between-habitat or "beta" diversity (see Whittaker 1975), is often high. The diversity of eucalypts in a region, called "gamma" diversity (see Kikkawa 1986), is therefore often high due to the high levels of alpha or beta diversity (or both) (see Wardell-Johnson et al. 1997).
Some regions of the continent display exceptionally high gamma diversity for eucalypts. For example, Beadle (1981) noted that the areas of greatest eucalypt species diversity on the continent include eastern New South Wales, and semi-arid to arid parts of southwestern Western Australia. Studies by Gill et al. (1985) and Kelly and Robson (1993) (based on analyses of records for eucalypt taxa recorded per 1:250,000 mapsheet, or per 1° latitude and longitude grid cell) identified three regions, including the east and southeast of the continent, the southwest of the continent extending into semi-arid regions, and the north and northeast of the continent, as having exceptionally high species diversity of eucalypts (see Gill et al. 1985, Table 2, p. 4 and Figure 2, p. 5; Kelly and Robson 1993, Map 7). The following summaries of eucalypt diversity for these three regions is largely derived from Wardell-Johnson et al. (1997) with reference to Gill et al. (1985).
The southeast of the continent, and particularly the sub-coastal region of central New South Wales including the Blue Mountains area, has one of the highest regional diversities for eucalypts of any part of the continent. For example, Gill et al. (1985) recorded 220 taxa with 111 endemic for the broader southeast region. Wardell-Johnson et al. (1997) recorded 84 taxa with 13 endemics for the sub-coastal region of central New South Wales bounded by the Hunter River valley to the north, the Blue Mountains area to the west and the Shoalhaven River area to the south. This area includes part of three biogeographic regions defined by Thackway and Cresswell (1995) including the Sydney Basin, the Southeast Corner and the East Coast and Ranges. Rates of eucalypt species changeover across the landscape (beta diversity) are particularly high for this region due to its topographic complexity and high levels of environmental heterogeneity, which result in a complex mosaic of habitats and environmental gradients.
The southwest region of the continent also displays exceptionally high gamma diversity for eucalypt species. Gill et al. (1985) recorded 223 eucalypt taxa for the broader southwest region, including 167 taxa and 75 endemics for the inland part which extends into the semi-arid and arid zones, and 56 taxa and 5 endemics for the far southwest corner extending from Albany to Perth. Wardell-Johnson et al. (1997) recorded 101 taxa with 31 endemics for the southwest corner of this broader region, defined by the Swan Coastal Plain, Jarrah Forest and Warren biogeographic regions of Thackway and Cresswell (1995). Heterogeneity of soil types rather than topographic factors is thought to be an important factor contributing to the high diversity of eucalypts in this region, resulting in a complex spatial mosaics of habitats. This complexity is reflected in the distribution of eucalypt species which include many endemic species and also some taxa that are largely peripheral to the region. The high regional diversity of eucalypts for the broader southwest of the continent occurs despite the fact that large parts of the region are dominated by vegetation which has relatively low diversities of eucalypts, such as the jarrah forest areas (see Bell and Heddle 1989).
The northeast of the continent is another region with high gamma diversity for the eucalypts. For example, Gill et al. (1985) recorded 130 eucalypt taxa with 31 endemics for the broader northeast part of the continent. Wardell-Johnson et al. (1997) recorded 65 taxa with 5 endemics for the central part of this region, defined as including parts of five of the biogeographic regions of Thackway and Cresswell (1995): the Wet Tropical Coast in the north, the Einasleigh Uplands in the west, the Brigalow Belt in the southeast, the Central Mackay Coast in the far southeast and the Desert Uplands in the far southwest. A combination of varied topographic features and climatic conditions has resulted in the wide range of habitats and high number of eucalypt species recorded for the northeast. These high levels of variation in habitat factors across the region are also associated with a high beta diversity for the eucalypts (Wardell-Johnson et al. 1997).
Factors that contribute to the exceptional diversity of each of these three regions include large numbers of eucalypt hybrids, endemics and rare species as well as the high levels of species diversity for particular eucalypt groups associated with each region. The eucalypt groups that contribute substantially to this diversity include: for the southeast - Monocalyptus and Symphyomyrtus (Section Maidenaria); for the southwest - Symphyomyrtus (Section Bisectaria); and for the northeast - Corymbia and Symphyomyrtus (Section Adnataria). In terms of rare species and endemics, the southwest region has 84 rare taxa and 31 endemic taxa amongst its eucalypt species, compared with 56 rare taxa and 13 endemic taxa for the southeast central region and 39 rare taxa and 5 endemic taxa for the northeast region (Wardell-Johnson et al. 1997, Table 5.2, p. 105). Estimates of numbers of hybrid taxa for these regions have also been made by Wardell-Johnson et al. (1997); these include 22 hybrid taxa for the southwest region, 74 for the southeast central region and 65 for the northeast region (see Table 5.2, p. 105)
The major eucalypt groups display high diversity, in terms of numbers of groups in a region, in parts of the northeast of the continent. For example, five of the informal subgenera of Eucalyptus sensu stricto, Angophora, and the two informal subgenera of Corymbia are found in the northeast (at Isla Gorge, Queensland). This high northeast diversity for eucalypt groups compares with 4 eucalypt subgenera and Angophora in the southeast, and 4 subgenera in the southwest (Wardell-Johnson et al. 1997).
Contribution to outstanding universal value: Taxonomic diversity
An important aspect in the evolutionary development of the eucalypts associated with their persistence and geographic expansion on the Australian continent is their extraordinary divergence, forming a monophyletic group of woody, dominant species of very high taxonomic diversity. The diversity of the eucalypts is comparable to the most diverse woody taxa found in the world and is also globally unusual in that it is almost entirely contained within one continent. Taxonomic diversity is an important aspect contributing to the outstanding universal value of the evolution of the eucalypts in Australia.
Places with exceptional regional diversity of eucalypt species are found in the southeast, southwest and northeast of the continent. The high regional diversity of these places results from very high levels of species replacement along environmental gradients, reflecting extraordinary levels of adaptation and evolutionary divergence of the eucalypts across catenae and complex spatial mosaics of changing environmental factors including soils, topography or microclimate. High levels of endemism, rarity, and hybridization, and also the retention of relictual taxa or “living fossils”, are important contributing factors to this exceptional regional diversity.