Renee A. Catullo

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.

Aridification drove repeated episodes of diversification between Australian biomes: Evidence from a multi-locus phylogeny of Australian toadlets (Uperoleia: Myobatrachidae)

Australia is a large and complex landmass that comprises diverse biomes ranging from tropical rainforests to harsh deserts. While Australian biotic diversity has evolved in response to landscape and climate changes, evidence of Miocene or later biome shifts are few. The Australo-Papuan endemic frog genus Uperoleia is widely distributed across mesic, monsoonal tropic and arid regions of Australia. Thus, it represents an ideal system to evaluate biome shifts as they relate to known landscape and climate history. We comprehensively sampled the distributional range of 25 described Uperoleia species and generated a detailed molecular phylogeny for the genus based on one mitochondrial and five nuclear loci. Our results support a single origin of monsoonal tropic taxa, followed by diversification within the region under the influence of the Australian monsoon. Molecular dating analyses suggest the major divergence between eastern mesic and monsoonal species occurred in the Miocene approximately 17million years ago, with repeated evolution of species from monsoonal biomes to arid or mesic biomes in the later Miocene, early Pliocene and at the beginning of the Pleistocene. Our detailed sampling helps to clarify the true distributions of species and contributes to on-going work to improve the taxonomy of the genus. Topological differences between nuclear and mitochondrial phylogenies within major clades suggest a history of mitochondrial introgression and capture, and reduce the ability to resolve close interspecific relationships.

Lineage range estimation method reveals fine-scale endemism linked to Pleistocene stability in Australian rainforest herpetofauna.

Areas of suitable habitat for species and communities have arisen, shifted, and disappeared with Pleistocene climate cycles, and through this shifting landscape, current biodiversity has found paths to the present. Evolutionary refugia, areas of relative habitat stability in this shifting landscape, support persistence of lineages through time, and are thus crucial to the accumulation and maintenance of biodiversity. Areas of endemism are indicative of refugial areas where diversity has persisted, and endemism of intraspecific lineages in particular is strongly associated with late-Pleistocene habitat stability. However, it remains a challenge to consistently estimate the geographic ranges of intraspecific lineages and thus infer phylogeographic endemism, because spatial sampling for genetic analyses is typically sparse relative to species records. We present a novel technique to model the geographic distribution of intraspecific lineages, which is informed by the ecological niche of a species and known locations of its constituent lineages. Our approach allows for the effects of isolation by unsuitable habitat, and captures uncertainty in the extent of lineage ranges. Applying this method to the arc of rainforest areas spanning 3500 km in eastern Australia, we estimated lineage endemism for 53 species of rainforest dependent herpetofauna with available phylogeographic data. We related endemism to the stability of rainforest habitat over the past 120,000 years and identified distinct concentrations of lineage endemism that can be considered putative refugia. These areas of lineage endemism are strongly related to historical stability of rainforest habitat, after controlling for the effects of current environment. In fact, a dynamic stability model that allows movement to track suitable habitat over time was the most important factor in explaining current patterns of endemism. The techniques presented here provide an objective, practical method for estimating geographic ranges below the species level, and including them in spatial analyses of biodiversity.

A new frog species (Myobatrachidae: Uperoleia ) from the Northern Deserts region of Australia, with a redescription of U. trachyderma

The frog genus Uperoleia (Myobatrachidae) is species rich, with the greatest diversity in the northern monsoonal region of Australia. Due in part to their small body size, conservative morphology and distribution in diverse habitats, the genus is likely to harbor cryptic species. A recent study (Catullo et al. 2013) assessed region-wide genetic, acoustic and phenotypic variation within four species in northern Australia. Catullo et al. (2013) presented multiple lines of evidence that the widespread U. trachyderma comprises distinct allopatric western and eastern lineages within the Northern Deserts bioregion of Australia. Here we formally describe the western lineage as U. stridera sp. nov. and redescribe the eastern (type) clade as U. trachyderma. The new species can be distinguished from U. trachyderma by fewer pulses per call, a faster pulse rate, and the lack of scattered orange to red flecks on the dorsum. The description of U. stridera sp. nov. brings the number of Uperoleia species to 28, by far the largest genus in the Myobatrachidae, and further highlights the Australian monsoonal tropics as a region of high endemism.

Resources for phylogenomic analyses of Australian terrestrial vertebrates

High‐throughput sequencing methods promise to improve our ability to infer the evolutionary histories of lineages and to delimit species. These are exciting prospects for the study of Australian vertebrates, a group comprised of many globally unique lineages with a long history of isolation. The evolutionary relationships within many of these lineages have been difficult to resolve with small numbers of loci, and we now know that many lineages also exhibit substantial cryptic diversity. Here, we present a set of phylogenetically diverse transcriptome resources to enable exon‐based sequence capture studies of Australian vertebrates, including transcriptome sequences for four species of birds, four frogs, seven lizards and seven mammals. We also use exon data from the marsupial transcriptomes we generated to examine an approach for choosing a moderate number (dozens or hundreds) of phylogenetically informative exons based on a single transcriptome sequence, and a relatively distant reference genome.

Phylogeographic structure across one of the largest intact tropical savannahs: Molecular and morphological analysis of Australia’s iconic frilled lizard Chlamydosaurus kingii

The spectacular threat display of the savannah specialist Australo-Papuan frilled lizards has made them one of the worlds most iconic reptiles. They are increasingly used as a model system for research in evolutionary biology and ecology but little is known of their population structure. Their distribution across northern Australia and southern New Guinea also provides an opportunity to examine biogeographic patterns as they relate to the large-scale movement of savannah habitat during the Plio/Pleistocene and the associated increase in aridity. We generated sequence data for one mitochondrial and four nuclear DNA loci (5052 base pairs) for 83 frilled lizards sampled throughout their range. We also quantified body proportion variation for 279 individuals. Phylogenetic analyses based on maximum likelihood and Bayesian species-tree methods revealed three shallow clades that replace each other across the monsoon tropics. We found the expected pattern of male biased sexual size dimorphism in both maximum body size and head size but there was no sexual dimorphism in overall body shape or in frill size, relative to head size, supporting the hypothesis that the frill is used primarily as a threat display rather than a sexual display. The genetic clades are broadly consistent with known clinal variation in frill color that gradually shifts from west to east (red, orange, yellow/white) but otherwise show little morphological differentiation in body proportion measures. The biogeographic breaks between clades occur at the Carpentaria Gap and the lowlands surrounding the Ord River, and our ecological niche modeling predicts lower habitat suitability for C. kingii in these regions. While this biogeographic pattern is consistent with numerous other taxonomic groups in northern Australia, the overall low genetic diversity in frilled lizards across the entire monsoon tropics and southern New Guinea contrasts starkly to patterns seen in other terrestrial vertebrates. Extremely low intra-clade genetic diversity over vast geographic areas is indicative of recent gene flow that would likely have been facilitated by widespread savannah during interglacials, or alternatively may reflect population bottlenecks induced by extreme aridity during Pleistocene glacials. The shallow divergence between Australian and New Guinean samples is consistent with recent connectivity between Australia and New Guinea that would have been possible via a savannah corridor across the Torres Strait. Based on our molecular and morphological data, we do not support taxonomic recognition of any of the frilled lizard clades and instead consider C. kingii a single species with shallow phylogeographic structure and clinal variation in frill color.

A new phylogenetic protocol: Dealing with model misspecification and confirmation bias in molecular phylogenetics

Molecular phylogenetics plays a key role in comparative genomics and has an increasingly-significant impacts on science, industry, government, public health, and society. In this opinion paper, we posit that the current phylogenetic protocol is missing two critical steps, and that their absence allows model misspecification and confirmation bias to unduly influence our phylogenetic estimates. Based on the potential offered by well-established but under-used procedures, such as assessment of phylogenetic assumptions and tests of goodness-of-fit, we introduce a new phylogenetic protocol that will reduce confirmation bias and increase the accuracy of phylogenetic estimates. Dedication To the memory of Rossiter H. Crozier (1943-2009), an evolutionary biologist, who, with his great generosity and wide-reaching inquisitiveness, inspired students and scientists in Australia, and abroad.