Leo Joseph

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.

Genome 10K: A Proposal to Obtain Whole-Genome Sequence for 10 000 Vertebrate Species

The human genome project has been recently complemented by whole-genome assessment sequence of 32 mammals and 24 nonmammalian vertebrate species suitable for comparative genomic analyses. Here we anticipate a precipitous drop in costs and increase in sequencing efficiency, with concomitant development of improved annotation technology and, therefore, propose to create a collection of tissue and DNA specimens for 10,000 vertebrate species specifically designated for whole-genome sequencing in the very near future. For this purpose, we, the Genome 10K Community of Scientists (G10KCOS), will assemble and allocate a biospecimen collection of some 16,203 representative vertebrate species spanning evolutionary diversity across living mammals, birds, nonavian reptiles, amphibians, and fishes (ca. 60,000 living species). In this proposal, we present precise counts for these 16,203 individual species with specimens presently tagged and stipulated for DNA sequencing by the G10KCOS. DNA sequencing has ushered in a new era of investigation in the biological sciences, allowing us to embark for the first time on a truly comprehensive study of vertebrate evolution, the results of which will touch nearly every aspect of vertebrate biological enquiry.

Declining body size: a third universal response to warming?

A recently documented correlate of anthropogenic climate change involves reductions in body size, the nature and scale of the pattern leading to suggestions of a third universal response to climate warming. Because body size affects thermoregulation and energetics, changing body size has implications for resilience in the face of climate change. A review of recent studies shows heterogeneity in the magnitude and direction of size responses, exposing a need for large-scale phylogenetically controlled comparative analyses of temporal size change. Integrative analyses of museum data combined with new theoretical models of size-dependent thermoregulatory and metabolic responses will increase both understanding of the underlying mechanisms and physiological consequences of size shifts and, therefore, the ability to predict the sensitivities of species to climate change.

Integrative taxonomy, or iterative taxonomy?

The recently introduced term ‘integrative taxonomy’ refers to taxonomy that integrates all available data sources to frame species limits. We survey current taxonomic methods available to delimit species that integrate a variety of data, including molecular and morphological characters. A literature review of empirical studies using the term ‘integrative taxonomy’ assessed the kinds of data being used to frame species limits, and methods of integration. Almost all studies are qualitative and comparative – we are a long way from a repeatable, quantitative method of truly ‘integrative taxonomy’. The usual methods for integrating data in phylogenetic and population genetic paradigms are not appropriate for integrative taxonomy, either because of the diverse range of data used or because of the special challenges that arise when working at the species/population boundary. We identify two challenges that, if met, will facilitate the development of a more complete toolkit and a more robust research programme in integrative taxonomy using species tree approaches. We propose the term ‘iterative taxonomy’ for current practice that treats species boundaries as hypotheses to be tested with new evidence. A search for biological or evolutionary explanations for discordant evidence can be used to distinguish between competing species boundary hypotheses. We identify two recent empirical examples that use the process of iterative taxonomy.

Phylogeography: its development and impact in Australo-Papuan ornithology with special reference to paraphyly in Australian birds

Abstract With examples from Australo-Papuan ornithology, we examine the technical and theoretical roots of molecular phylogeography and review its development. We describe the progression from ad hoc interpretation of gene trees in single species phylogeographic studies through to comparative phylogeography and currently advocated model-testing approaches. Mitochondrial DNA (mtDNA) sequences have provided most advances to date, although we demonstrate and advocate the future use of multilocus datasets analysed with coalescent methods. We examine interrelationships among speciation research, historical biogeography, phylogeography and landscape genetics. Mitochondrial paraphyly, in which individuals of one species or population have mtDNA that is more closely related to that of another than to their own, emerges in 44% of Australian studies to date as a common, important result in Australian avian phylogeography. Accordingly, we explore at length its most common causes and its impact on case studies in Australo-Papuan avian phylogeography. The impact of so much paraphyly on avian phylogeography and taxonomy is a major theme of the review. We suggest a full research agenda for avian phylogeography in the Australo-Papuan region that spans diverse topics: the need for more studies of pelagic birds, spatio-temporal links between New Guinea and Australia, island populations, testing of long-established biogeographical hypotheses, and integration of molecular and non-molecular datasets into integrated evolutionary understanding of species and populations. Studying the full continuum of divergences from landscape genetics, to phylogeography, to recently diverged species with evidence of paraphyly, to highly divergent species with many fixed differences will lead to a more complete understanding of the processes and patterns of avian evolution.

A framework for incorporating evolutionary genomics into biodiversity conservation and management

Evolutionary adaptation drives biodiversity. So far, however, evolutionary thinking has had limited impact on plans to counter the effects of climate change on biodiversity and associated ecosystem services. This is despite habitat fragmentation diminishing the ability of populations to mount evolutionary responses, via reductions in population size, reductions in gene flow and reductions in the heterogeneity of environments that populations occupy. Research on evolutionary adaptation to other challenges has benefitted enormously in recent years from genomic tools, but these have so far only been applied to the climate change issue in a piecemeal manner. Here, we explore how new genomic knowledge might be combined with evolutionary thinking in a decision framework aimed at reducing the long-term impacts of climate change on biodiversity and ecosystem services. This framework highlights the need to rethink local conservation and management efforts in biodiversity conservation. We take a dynamic view of biodiversity based on the recognition of continuously evolving lineages, and we highlight when and where new genomic approaches are justified. In general, and despite challenges in developing genomic tools for non-model organisms, genomics can help management decide when resources should be redirected to increasing gene flow and hybridisation across climate zones and facilitating in situ evolutionary change in large heterogeneous areas. It can also help inform when conservation priorities need to shift from maintaining genetically distinct populations and species to supporting processes of evolutionary change. We illustrate our argument with particular reference to Australia’s biodiversity.

Shifting latitudinal clines in avian body size correlate with global warming in Australian passerines

Intraspecific latitudinal clines in the body size of terrestrial vertebrates, where members of the same species are larger at higher latitudes, are widely interpreted as evidence for natural selection and adaptation to local climate. These clines are predicted to shift in response to climate change. We used museum specimens to measure changes in the body size of eight passerine bird species from south-eastern Australia over approximately the last 100 years. Four species showed significant decreases in body size (1.8–3.6% of wing length) and a shift in latitudinal cline over that period, and a meta-analysis demonstrated a consistent trend across all eight species. Southern high-latitude populations now display the body sizes typical of more northern populations pre-1950, equivalent to a 7° shift in latitude. Using ptilochronology, we found no evidence that these morphological changes were a plastic response to changes in nutrition, a likely non-genetic mechanism for the pattern observed. Our results demonstrate a generalized response by eight avian species to some major environmental change over the last 100 years or so, probably global warming.

Multilocus analysis of honeyeaters (Aves: Meliphagidae) highlights spatio‐temporal heterogeneity in the influence of biogeographic barriers in the Australian monsoonal zone

Multilocus studies in phylogenetics and comparative phylogeography have the power to explore a broader spectrum of evolutionary questions than either discipline has alone. To examine the origins of sympatry in a group of closely related birds of mostly mesic eucalypt woodlands in Australia, we reconstructed the relationships among species of Entomyzon and Melithreptus honeyeaters (Aves: Passeriformes: Meliphagidae) using a mitochondrial marker, ND2, and six non‐coding nuclear loci (total 4719 base pairs). By sampling across the geographical range of each species, we studied not only their phylogenetic relationships to each other but also the spatial distribution of their genetic diversity. We tested several biogeographic hypotheses concerning the role of Pleistocene environmental change in Australia. Phylogenetic gene trees support the current understanding of E. cyanotis as the sister to Melithreptus. Non‐monophyly of M. lunatus in Australia’s southern temperate woodlands highlights the need for a revision of systematics within Melithreptus. Phylogeographic analysis of the three northern species in Australia’s monsoon tropics, M. gularis, M. albogularis and E. cyanotis, suggests that the roles of the Carpentarian and Torresian Barriers in shaping geographic structure in each of the species have been more complex and temporally dynamic than earlier morphology‐based arguments of vicariance had suggested. We discuss their roles as ecological filters as well as barriers.

Perched at the mito-nuclear crossroads: divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear gene flow in an Australian bird.

Relationships among multilocus genetic variation, geography, and environment can reveal how evolutionary processes affect genomes. We examined the evolution of an Australian bird, the eastern yellow robin Eopsaltria australis, using mitochondrial (mtDNA) and nuclear (nDNA) genetic markers, and bioclimatic variables. In southeastern Australia, two divergent mtDNA lineages occur east and west of the Great Dividing Range, perpendicular to latitudinal nDNA structure. We evaluated alternative scenarios to explain this striking discordance in landscape genetic patterning. Stochastic mtDNA lineage sorting can be rejected because the mtDNA lineages are essentially distinct geographically for > 1500 km. Vicariance is unlikely: the Great Dividing Range is neither a current barrier nor was it at the Last Glacial Maximum according to species distribution modeling; nuclear gene flow inferred from coalescent analysis affirms this. Female philopatry contradicts known female‐biased dispersal. Contrasting mtDNA and nDNA demographies indicate their evolutionary histories are decoupled. Distance‐based redundancy analysis, in which environmental temperatures explain mtDNA variance above that explained by geographic position and isolation‐by‐distance, favors a nonneutral explanation for mitochondrial phylogeographic patterning. Thus, observed mito‐nuclear discordance accords with environmental selection on a female‐linked trait, such as mtDNA, mtDNA–nDNA interactions or genes on W‐chromosome, driving mitochondrial divergence in the presence of nuclear gene flow.

Phylogeny and evolution of the Meliphagoidea, the largest radiation of Australasian songbirds

The Meliphagoidea comprises the largest radiation of Australasian passerines. Here we present the first detailed molecular phylogenetic analysis of its families and genera, particularly the Acanthizidae, using sequences from nine gene regions including both mitochondrial and nuclear DNA. Our results support some suggested relationships but challenge other groupings, particularly in Meliphagidae and Acanthizidae. Maluridae is sister to all other members of the superfamily. With appropriate taxon sampling and multilocus data, we provide the first strong molecular evidence supporting earlier recognition of bristlebirds, Dasyornis, as a separate family, Dasyornithidae. We further clarify its position as sister to Acanthizidae+Pardalotidae+Meliphagidae. Pardalotidae is sister to Acanthizidae, and thus its retention as a separate family is arbitrary. The meliphagid genus Lichenostomus is polyphyletic. We find no support for the current subfamily structure within Acanthizidae but recognise a clade that includes members of the subfamily Sericornithinae excluding Oreoscopus and Acanthornis. Subfamily Acanthizinae is paraphyletic. Surprisingly, the Tasmanian island endemic Acanthornis magna of mesic habitats is sister to the Aphelocephala whitefaces of mainland Australian xeric zones. This is one of several unexpected alignments of taxa as sisters that probably reflects the age of the Meliphagoidea. We find no evidence for separate radiations of New Guinean and Australian members of the Meliphagoidea.