Andrew H. Thornhill

Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary

Fire is a major modifier of communities, but the evolutionary origins of its prevalent role in shaping current biomes are uncertain. Australia is among the most fire-prone continents, with most of the landmass occupied by the fire-dependent sclerophyll and savanna biomes. In contrast to biomes with similar climates in other continents, Australia has a tree flora dominated by a single genus, Eucalyptus, and related Myrtaceae. A unique mechanism in Myrtaceae for enduring and recovering from fire damage likely resulted in this dominance. Here, we find a conserved phylogenetic relationship between post-fire resprouting (epicormic) anatomy and biome evolution, dating from 60 to 62 Ma, in the earliest Palaeogene. Thus, fire-dependent communities likely existed 50 million years earlier than previously thought. We predict that epicormic resprouting could make eucalypt forests and woodlands an excellent long-term carbon bank for reducing atmospheric CO(2) compared with biomes with similar fire regimes in other continents.

Phylogenetic measures of biodiversity and neo- and paleo-endemism in Australian Acacia

Understanding spatial patterns of biodiversity is critical for conservation planning, particularly given rapid habitat loss and human-induced climatic change. Diversity and endemism are typically assessed by comparing species ranges across regions. However, investigation of patterns of species diversity alone misses out on the full richness of patterns that can be inferred using a phylogenetic approach. Here, using Australian Acacia as an example, we show that the application of phylogenetic methods, particularly two new measures, relative phylogenetic diversity and relative phylogenetic endemism, greatly enhances our knowledge of biodiversity across both space and time. We found that areas of high species richness and species endemism are not necessarily areas of high phylogenetic diversity or phylogenetic endemism. We propose a new method called categorical analysis of neo- and paleo-endemism (CANAPE) that allows, for the first time, a clear, quantitative distinction between centres of neo- and paleo-endemism, useful to the conservation decision-making process.

Are pollen fossils useful for calibrating relaxed molecular clock dating of phylogenies? A comparative study using Myrtaceae.

The identification and application of reliable fossil calibrations represents a key component of many molecular studies of evolutionary timescales. In studies of plants, most paleontological calibrations are associated with macrofossils. However, the pollen record can also inform age calibrations if fossils matching extant pollen groups are found. Recent work has shown that pollen of the myrtle family, Myrtaceae, can be classified into a number of morphological groups that are synapomorphic with molecular groups. By assembling a data matrix of pollen morphological characters from extant and fossil Myrtaceae, we were able to measure the fit of 26 pollen fossils to a molecular phylogenetic tree using parsimony optimisation of characters. We identified eight Myrtaceidites fossils as appropriate for calibration based on the most parsimonious placements of these fossils on the tree. These fossils were used to inform age constraints in a Bayesian phylogenetic analysis of a sequence alignment comprising two sequences from the chloroplast genome (matK and ndhF) and one nuclear locus (ITS), sampled from 106 taxa representing 80 genera. Three additional analyses were calibrated by placing pollen fossils using geographic and morphological information (eight calibrations), macrofossils (five calibrations), and macrofossils and pollen fossils in combination (12 calibrations). The addition of new fossil pollen calibrations led to older crown ages than have previously been found for tribes such as Eucalypteae and Myrteae. Estimates of rate variation among lineages were affected by the choice of calibrations, suggesting that the use of multiple calibrations can improve estimates of rate heterogeneity among lineages. This study illustrates the potential of including pollen-based calibrations in molecular studies of divergence times.

Interpreting the modern distribution of Myrtaceae using a dated molecular phylogeny

The angiosperm family Myrtaceae has extant and fossil taxa from all southern continents and is assumed to be of Gondwanan origin. Many modern groups contain sister taxa that have disjunct transoceanic distributions, which can be interpreted as a result of either vicariance or long-distance dispersal and establishment (LDDE). Further, some Myrtaceae groups occur on Pacific islands with enigmatic geological histories. We tested hypotheses of vicariance and LDDE by estimating divergence times using a relaxed molecular clock calibrated with 12 fossils. In total, 88 genera and 202 species were sampled, representing both subfamilies and all tribes of Myrtaceae. We reconstructed the family as Gondwanan in origin. Of the 22 geographically disjunct sister groups in our study, up to six are potentially explained as the product of vicariance, three resulting from overland dispersal via new land connections, and 13 due to LDDE events. Nine of the 13 hypothesized LDDE events occurred in fleshy-fruited taxa. Our results indicate that most of the transoceanic distribution patterns in Myrtaceae have occurred since the Miocene due to LDDE, whereas inferred vicariance events all occurred before the Late Eocene. There are many instances of sister relationships between species-poor and species-rich groups in Myrtaceae, and at least three occurrences of geographically isolated taxa on long branches of the phylogeny (Arillastrum, Myrtus, and Tepualia), whose modern-day distributions are difficult to explain without additional fossil or geological evidence.

Phylogenetic diversity meets conservation policy: Small areas are key to preserving eucalypt lineages

Evolutionary and genetic knowledge is increasingly being valued in conservation theory, but is rarely considered in conservation planning and policy. Here, we integrate phylogenetic diversity (PD) with spatial reserve prioritization to evaluate how well the existing reserve system in Victoria, Australia captures the evolutionary lineages of eucalypts, which dominate forest canopies across the state. Forty-three per cent of remaining native woody vegetation in Victoria is located in protected areas (mostly national parks) representing 48% of the extant PD found in the state. A modest expansion in protected areas of 5% (less than 1% of the state area) would increase protected PD by 33% over current levels. In a recent policy change, portions of the national parks were opened for development. These tourism development zones hold over half the PD found in national parks with some species and clades falling entirely outside of protected zones within the national parks. This approach of using PD in spatial prioritization could be extended to any clade or area that has spatial and phylogenetic data. Our results demonstrate the relevance of PD to regional conservation policy by highlighting that small but strategically located areas disproportionally impact the preservation of evolutionary lineages.

Quantifying Phytogeographical Regions of Australia Using Geospatial Turnover in Species Composition

The largest digitized dataset of land plant distributions in Australia assembled to date (750,741 georeferenced herbarium records; 6,043 species) was used to partition the Australian continent into phytogeographical regions. We used a set of six widely distributed vascular plant groups and three non-vascular plant groups which together occur in a variety of landscapes/habitats across Australia. Phytogeographical regions were identified using quantitative analyses of species turnover, the rate of change in species composition between sites, calculated as Simpsons beta. We propose six major phytogeographical regions for Australia: Northern, Northern Desert, Eremaean, Eastern Queensland, Euronotian and South-Western. Our new phytogeographical regions show a spatial agreement of 65% with respect to previously defined phytogeographical regions of Australia. We also confirm that these new regions are in general agreement with the biomes of Australia and other contemporary biogeographical classifications. To assess the meaningfulness of the proposed phytogeographical regions, we evaluated how they relate to broad scale environmental gradients. Physiographic factors such as geology do not have a strong correspondence with our proposed regions. Instead, we identified climate as the main environmental driver. The use of an unprecedentedly large dataset of multiple plant groups, coupled with an explicit quantitative analysis, makes this study novel and allows an improved historical bioregionalization scheme for Australian plants. Our analyses show that: (1) there is considerable overlap between our results and older biogeographic classifications; (2) phytogeographical regions based on species turnover can be a powerful tool to further partition the landscape into meaningful units; (3) further studies using phylogenetic turnover metrics are needed to test the taxonomic areas.

Pollen morphology of the Myrtaceae. Part 1: tribes Eucalypteae, Lophostemoneae, Syncarpieae, Xanthostemoneae and subfamily Psiloxyloideae

A family-wide palynological study of Myrtaceae was conducted using scanning electron microscopy (SEM) and light microscopy (LM). In this part of the study, the pollen morphology of 18 genera and 150 species from the Myrtaceae tribes of subfamily Myrtoideae, Eucalypteae, Lophostemoneae, Syncarpieae, Xanthostemoneae and subfamily Psiloxyloideae are presented. It was found that the most commonly observed pollen in these groups was parasyncolpate with a rugulate exine, whereas some species possessed an apocolpial island. The large, and sometimes syndemicolpate, pollen of Eucalypteae genera Angophora and Corymbia differed from all other genera. Most Eucalyptus pollen had endopores with a thickened exine.

Salt- and alkaline-tolerance are linked in Acacia

Saline or alkaline soils present a strong stress on plants that together may be even more deleterious than alone. Australias soils are old and contain large, sometimes overlapping, areas of high salt and alkalinity. Acacia and other Australian plant lineages have evolved in this stressful soil environment and present an opportunity to understand the evolution of salt and alkalinity tolerance. We investigate this evolution by predicting the average soil salinity and pH for 503 Acacia species and mapping the response onto a maximum-likelihood phylogeny. We find that salinity and alkalinity tolerance have evolved repeatedly and often together over 25 Ma of the Acacia radiation in Australia. Geographically restricted species are often tolerant of extreme conditions. Distantly related species are sympatric in the most extreme soil environments, suggesting lack of niche saturation. There is strong evidence that many Acacia have distributions affected by salinity and alkalinity and that preference is lineage specific.

Pollen morphology of the Myrtaceae. Part 4: tribes Kanieae, Myrteae and Tristanieae

Pollen morphology of 44 genera and 101 species from the Myrtaceae tribes Kanieae, Myrteae and Tristanieae was surveyed using scanning electron microscopy (SEM) and light microscopy (LM). Most Myrteae pollen were brevicolpate and granulate, which is unique within Myrtaceae, and these are most likely ancestral characters for this tribe. Two main pollen types were observed in tribe Kanieae, one form being with syncolpate colpi and a distinctive granulate exine, and the other with parasyncolpate colpi and a less ornamented exine. Genera Tristania and Thaleropia of tribe Tristanieae produce the smallest pollen in Myrtaceae, whereas Octamyrtus of tribe Myrteae produces the largest pollen observed in Myrtaceae.

Continental scale patterns and predictors of fern richness and phylogenetic diversity

Because ferns have a wide range of habitat preferences and are widely distributed, they are an ideal group for understanding how diversity is distributed. Here we examine fern diversity on a broad-scale using standard and corrected richness measures as well as phylogenetic indices; in addition we determine the environmental predictors of each diversity metric. Using the combined records of Australian herbaria, a dataset of over 60,000 records was obtained for 89 genera to infer richness. A molecular phylogeny of all the genera was constructed and combined with the herbarium records to obtain phylogenetic diversity patterns. A hotspot of both taxic and phylogenetic diversity occurs in the Wet Tropics of northeastern Australia. Although considerable diversity is distributed along the eastern coast, some important regions of diversity are identified only after sample-standardization of richness and through the phylogenetic metric. Of all of the metrics, annual precipitation was identified as the most explanatory variable, in part, in agreement with global and regional fern studies. However, precipitation was combined with a different variable for each different metric. For corrected richness, precipitation was combined with temperature seasonality, while correlation of phylogenetic diversity to precipitation plus radiation indicated support for the species-energy hypothesis. Significantly high and significantly low phylogenetic diversity were found in geographically separate areas. These separate areas correlated with different climatic conditions such as seasonality in precipitation. The phylogenetic metrics identified additional areas of significant diversity, some of which have not been revealed using traditional taxonomic analyses, suggesting that different ecological and evolutionary processes have operated over the continent. Our study demonstrates that it is possible and vital to incorporate evolutionary metrics when inferring biodiversity hotspots from large compilations of data.