Stephen C. Donnellan

Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota

The integration of phylogenetics, phylogeography and palaeoenvironmental studies is providing major insights into the historical forces that have shaped the Earths biomes. Yet our present view is biased towards arctic and temperate/tropical forest regions, with very little focus on the extensive arid regions of the planet. The Australian arid zone is one of the largest desert landform systems in the world, with a unique, diverse and relatively well-studied biota. With foci on palaeoenvironmental and molecular data, we here review what is known about the assembly and maintenance of this biome in the context of its physical history, and in comparison with other mesic biomes. Aridification of Australia began in the Mid-Miocene, around 15 million years, but fully arid landforms in central Australia appeared much later, around 1-4 million years. Dated molecular phylogenies of diverse taxa show the deepest divergences of arid-adapted taxa from the Mid-Miocene, consistent with the onset of desiccation. There is evidence of arid-adapted taxa evolving from mesic-adapted ancestors, and also of speciation within the arid zone. There is no evidence for an increase in speciation rate during the Pleistocene, and most arid-zone species lineages date to the Pliocene or earlier. The last 0.8 million years have seen major fluctuations of the arid zone, with large areas covered by mobile sand dunes during glacial maxima. Some large, vagile taxa show patterns of recent expansion and migration throughout the arid zone, in parallel with the ice sheet-imposed range shifts in Northern Hemisphere taxa. Yet other taxa show high lineage diversity and strong phylogeographical structure, indicating persistence in multiple localised refugia over several glacial maxima. Similar to the Northern Hemisphere, Pleistocene range shifts have produced suture zones, creating the opportunity for diversification and speciation through hybridisation, polyploidy and parthenogenesis. This review highlights the opportunities that development of arid conditions provides for rapid and diverse evolutionary radiations, and re-enforces the emerging view that Pleistocene environmental change can have diverse impacts on genetic structure and diversity in different biomes. There is a clear need for more detailed and targeted phylogeographical studies of Australias arid biota and we suggest a framework and a set of a priori hypotheses by which to proceed.

Exceptional among-lineage variation in diversification rates during the radiation of Australia's most diverse vertebrate clade

The disparity in species richness among groups of organisms is one of the most pervasive features of life on earth. A number of studies have addressed this pattern across higher taxa (e.g. ‘beetles’), but we know much less about the generality and causal basis of the variation in diversity within evolutionary radiations at lower taxonomic scales. Here, we address the causes of variation in species richness among major lineages of Australias most diverse vertebrate radiation, a clade of at least 232 species of scincid lizards. We use new mitochondrial and nuclear intron DNA sequences to test the extent of diversification rate variation in this group. We present an improved likelihood-based method for estimating per-lineage diversification rates from combined phylogenetic and taxonomic (species richness) data, and use the method in a hypothesis-testing framework to localize diversification rate shifts on phylogenetic trees. We soundly reject homogeneity of diversification rates among members of this radiation, and find evidence for a dramatic rate increase in the common ancestor of the genera Ctenotus and Lerista. Our results suggest that the evolution of traits associated with climate tolerance may have had a role in shaping patterns of diversity in this group.

Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history

We present a new, broadly applicable measure of the spatial restriction of phylogenetic diversity, termed phylogenetic endemism (PE). PE combines the widely used phylogenetic diversity and weighted endemism measures to identify areas where substantial components of phylogenetic diversity are restricted. Such areas are likely to be of considerable importance for conservation. PE has a number of desirable properties not combined in previous approaches. It assesses endemism consistently, independent of taxonomic status or level, and independent of previously defined political or biological regions. The results can be directly compared between areas because they are based on equivalent spatial units. PE builds on previous phylogenetic analyses of endemism, but provides a more general solution for mapping endemism of lineages. We illustrate the broad applicability of PE using examples of Australian organisms having contrasting life histories: pea‐flowered shrubs of the genus Daviesia (Fabaceae) and the Australian species of the Australo‐Papuan tree frog radiation within the family Hylidae.

Multiple geographic origins of commensalism and complex dispersal history of black rats

The Black Rat (Rattus rattus) spread out of Asia to become one of the worlds worst agricultural and urban pests, and a reservoir or vector of numerous zoonotic diseases, including the devastating plague. Despite the global scale and inestimable cost of their impacts on both human livelihoods and natural ecosystems, little is known of the global genetic diversity of Black Rats, the timing and directions of their historical dispersals, and the risks associated with contemporary movements. We surveyed mitochondrial DNA of Black Rats collected across their global range as a first step towards obtaining an historical genetic perspective on this socioeconomically important group of rodents. We found a strong phylogeographic pattern with well-differentiated lineages of Black Rats native to South Asia, the Himalayan region, southern Indochina, and northern Indochina to East Asia, and a diversification that probably commenced in the early Middle Pleistocene. We also identified two other currently recognised species of Rattus as potential derivatives of a paraphyletic R. rattus. Three of the four phylogenetic lineage units within R. rattus show clear genetic signatures of major population expansion in prehistoric times, and the distribution of particular haplogroups mirrors archaeologically and historically documented patterns of human dispersal and trade. Commensalism clearly arose multiple times in R. rattus and in widely separated geographic regions, and this may account for apparent regionalism in their associated pathogens. Our findings represent an important step towards deeper understanding the complex and influential relationship that has developed between Black Rats and humans, and invite a thorough re-examination of host-pathogen associations among Black Rats.

Analysis and visualization of complex Macroevolutionary dynamics: An example from Australian Scincid lizards

The correlation between species diversification and morphological evolution has long been of interest in evolutionary biology. We investigated the relationship between these processes during the radiation of 250+scincid lizards that constitute Australias most species-rich clade of terrestrial vertebrates. We generated a time-calibrated phylogenetic tree for the group that was more than 85% complete at the species level and collected multivariate morphometric data for 183 species. We reconstructed the dynamics of species diversification and trait evolution using a Bayesian statistical framework (BAMM) that simultaneously accounts for variation in evolutionary rates through time and among lineages. We extended the BAMM model to accommodate time-dependent phenotypic evolution, and we describe several new methods for summarizing and visualizing macroevolutionary rate heterogeneity on phylogenetic trees. Two major clades (Lerista, Ctenotus; >90 spp. each) are associated with high rates of species diversification relative to the background rate across Australian sphenomorphine skinks. The Lerista clade is characterized by relatively high lability of body form and has undergone repeated instances of limb reduction, but Ctenotus is characterized by an extreme deceleration in the rate of body shape evolution. We estimate that rates of phenotypic evolution decreased by more than an order of magnitude in the common ancestor of the Ctenotus clade. These results provide evidence for a modal shift in phenotypic evolutionary dynamics and demonstrate that major axes of morphological variation can be decoupled from species diversification. More generally, the Bayesian framework described here can be used to identify and characterize complex mixtures of dynamic processes on phylogenetic trees. [Bayesian; diversification; evolvability; lizard; macroevolution, punctuated equilibrium, speciation.].

Diversification and persistence at the arid-monsoonal interface: Australia-wide biogeography of the bynoe's gecko (heteronotia binoei; gekkonidae)

Late Neogene aridification in the Southern Hemisphere caused contractions of mesic biota to refugia, similar to the patterns established by glaciation in the Northern Hemisphere, but these episodes also opened up new adaptive zones that spurred range expansion and diversification in arid‐adapted lineages. To understand these dynamics, we present a multilocus (nine nuclear introns, one mitochondrial gene) phylogeographic analysis of the Bynoes gecko (Heteronotia binoei), a widely distributed complex spanning the tropical monsoon, coastal woodland, and arid zone biomes in Australia. Bayesian phylogenetic analyses, estimates of divergence times, and demographic inferences revealed episodes of diversification in the Pliocene, especially in the tropical monsoon biome, and range expansions in the Pleistocene. Ancestral habitat reconstructions strongly support recent and independent invasions into the arid zone. Our study demonstrates the varied responses to aridification in Australia, including localized persistence of lineages in the tropical monsoonal biome, and repeated invasion of and expansion through newly available arid‐zone habitats. These patterns are consistent with those found in other arid environments in the Southern Hemisphere, including the South African succulent karoo and the Chilean lowlands, and highlight the diverse modes of diversification and persistence of Earths biota during the glacial cycles of the Pliocene and Pleistocene.

Phylogeographic analysis of the green python, Morelia viridis, reveals cryptic diversity.

Green pythons, which are regionally variable in colour patterns, are found throughout the lowland rainforest of New Guinea and adjacent far northeastern Australia. The species is popular in commercial trade and management of this trade and its impacts on natural populations could be assisted by molecular identification tools. We used mitochondrial nucleotide sequences and a limited allozyme data to test whether significantly differentiated populations occur within the species range. Phylogenetic analysis of mtDNA sequences revealed hierarchal phylogeographic structure both within New Guinea and between New Guinea and Australia. Strongly supported reciprocally monophyletic mitochondrial lineages, northern and southern, were found either side of the central mountain range that runs nearly the length of New Guinea. Limited allozyme data suggest that population differentiation is reflected in the nuclear as well as the mitochondrial genome. A previous morphological analysis did not find any phenotypic concordance with the pattern of differentiation observed in the molecular data. The southern mitochondrial lineage includes all of the Australian haplotypes, which form a single lineage, nested among the southern New Guinean haplotypes.

Molecular Phylogeny, Biogeography, and Habitat Preference Evolution of Marsupials

Marsupials exhibit great diversity in ecology and morphology. However, compared with their sister group, the placental mammals, our understanding of many aspects of marsupial evolution remains limited. We use 101 mitochondrial genomes and data from 26 nuclear loci to reconstruct a dated phylogeny including 97% of extant genera and 58% of modern marsupial species. This tree allows us to analyze the evolution of habitat preference and geographic distributions of marsupial species through time. We found a pattern of mesic-adapted lineages evolving to use more arid and open habitats, which is broadly consistent with regional climate and environmental change. However, contrary to the general trend, several lineages subsequently appear to have reverted from drier to more mesic habitats. Biogeographic reconstructions suggest that current views on the connectivity between Australia and New Guinea/Wallacea during the Miocene and Pliocene need to be revised. The antiquity of several endemic New Guinean clades strongly suggests a substantially older period of connection stretching back to the Middle Miocene and implies that New Guinea was colonized by multiple clades almost immediately after its principal formation.

Interspecies sequence differences in the Mip protein from the genus Legionella: implications for function and evolutionary relatedness

The nucleotide sequence of the mip genes and their inferred amino acid sequences were determined from 35 Legionella species and compared with the published sequences for L. pneumophila, L. micdadei and L. longbeachae. The sequences were 69–97% conserved at the nucleotide level and 82–99% at the amino acid level, with total conservation of amino acids determined to be associated with sites known to be involved in peptidyl prolyl cis–trans isomerase activity. No apparent difference could be determined in the arrangement of amino acids that would predict a functional difference in Mip from species associated with disease and Mip from species isolated only from the environment. Additionally, a phylogenetic comparison of the sequences with published 16S RNA sequences, using both genetic distance and maximum parsimony methods, was performed. Few relationships were apparent that were well supported by both data sets, the most robust being a clade comprising {[(cincinnatiensis, longbeachae, sainthelensi, santicrucis) gratiana] (moravica, quateirensis, shakespearei, worsleiensis) anisa, bozemanii, cherrii, dumoffii, gormanii, jordanis, parisiensis, pneumophila, steigerwaltii, tucsonensis, and wadsworthii }.

Cold Code: the global initiative to DNA barcode amphibians and nonavian reptiles

DNA barcoding facilitates the identification of species and the estimation of biodiversity by using nucleotide sequences, usually from the mitochondrial genome. Most studies accomplish this task by using the gene encoding cytochrome oxidase subunit I (COI; Entrez COX1). Within this barcoding framework, many taxonomic initiatives exist, such as those specializing in fishes, birds, mammals, and fungi. Other efforts center on regions, such as the Arctic, or on other topics, such as health. DNA barcoding initiatives exist for all groups of vertebrates except for amphibians and nonavian reptiles. We announce the formation of Cold Code, the international initiative to DNA barcode all species of these ‘cold‐blooded’ vertebrates. The project has a Steering Committee, Coordinators, and a home page. To facilitate Cold Code, the Kunming Institute of Zoology, Chinese Academy of Sciences will sequence COI for the first 10 specimens of a species at no cost to the steward of the tissues.