Protecting Biodiversity (in All Its Complexity): New Models and Methods.

We are facing a biodiversity crisis at the same time as we are acquiring an unprecedented view of the world's biodiversity. Vast new datasets (e.g., species distributions, traits, phylogenies, and interaction networks) hold knowledge to better comprehend the depths of biodiversity change, reliably anticipate these changes, and inform conservation actions. To harness this information for conservation, we need to integrate the largely independent fields of biodiversity modeling and conservation. We highlight new developments in each respective field, early examples of how they are being brought together, and ideas for a future synthesis such that conservation decisions can be made with fuller awareness of the biodiversity at stake.

Pleistocene climatic changes drive diversification across a tropical savanna.

Spatial responses of species to past climate change depend on both intrinsic traits (climatic niche breadth, dispersal rates) and the scale of climatic fluctuations across the landscape. New capabilities in generating and analysing population genomic data, along with spatial modelling, have unleashed our capacity to infer how past climate changes have shaped populations, and by extension, complex communities. Combining these approaches, we uncover lineage diversity across four codistributed lizards from the Australian Monsoonal Tropics and explore how varying climatic tolerances interact with regional climate history to generate common vs. disparate responses to late Pleistocene change. We find more divergent spatial structuring and temporal demographic responses in the drier Kimberley region compared to the more mesic and consistently suitable Top End. We hypothesize that, in general, the effects of species' traits on sensitivity to climate fluctuation will be more evident in climatically marginal regions. If true, this points to the need in climatically marginal areas to craft more species-(or trait)-specific strategies for persistence under future climate change.

Phylogenetically informed spatial planning is required to conserve the mammalian tree of life.

In the face of the current extinction crisis and severely limited conservation resources, safeguarding the tree of life is increasingly recognized as a high priority. We conducted a first systematic global assessment of the conservation of phylogenetic diversity (PD) that uses realistic area targets and highlights the key areas for conservation of the mammalian tree of life. Our approach offers a substantially more effective conservation solution than one focused on species. In many locations, priorities for PD differ substantially from those of a species-based approach that ignores evolutionary relationships. This discrepancy increases rapidly as the amount of land available for conservation declines, as does the relative benefit for mammal conservation (for the same area protected). This benefit is equivalent to an additional 5900 Myr of distinct mammalian evolution captured simply through a better informed choice of priority areas. Our study uses area targets for PD to generate more realistic conservation scenarios, and tests the impact of phylogenetic uncertainty when selecting areas to represent diversity across a phylogeny. It demonstrates the opportunity of using rapidly growing phylogenetic information in conservation planning and the readiness for a new generation of conservation planning applications that explicitly consider the heritage of the tree of life's biodiversity.

Trans-biome diversity in Australian grass-specialist lizards (Diplodactylidae: Strophurus).

Comparisons of biodiversity patterns within lineages that occur across major climate gradients and biomes, can provide insights into the relative roles that lineage history, landscape and climatic variation, and environmental change have played in shaping regional biotas. In Australia, while there has been extensive research into the origins and patterns of diversity in the Australian Arid Zone (AAZ), how diversity is distributed across this biome and the Australian Monsoonal Tropics (AMT) to the north, has been less studied. We compared the timing and patterns of diversification across this broad aridity gradient in a clade of lizards (Strophurus: phasmid geckos) that only occur in association with a unique Australian radiation of sclerophyllous grasses (Triodia: spinifex). Our results indicate that overall genetic diversity is much higher, older and more finely geographically structured within the AMT, including distantly related clades endemic to the sandstone escarpments of the Kimberley and Arnhem Plateau. Niche modelling analyses also suggest that the distribution of taxa in the AMT is more strongly correlated with variation in topographic relief than in the AAZ. The two broad patterns that we recovered - (i) lineage endemism increases as latitude decreases, and (ii) endemism is tightly correlated to rocky regions - parallel and corroborate other recent studies of habitat generalists and specialised saxicoline lineages occurring across these same regions. Early Miocene diversification estimates also suggest that, soon after Triodia grasses colonised Australia and began to diversify in the Miocene, phasmid geckos with Gondwanan ancestry shifted into these grasses, and have subsequently remained closely associated with this unique vegetation type.

Correction: Lineage Range Estimation Method Reveals Fine-Scale Endemism Linked to Pleistocene Stability in Australian Rainforest Herpetofauna.

[This corrects the article DOI: 10.1371/journal.pone.0126274.].

A guide to phylogenetic metrics for conservation, community ecology and macroecology.

The use of phylogenies in ecology is increasingly common and has broadened our understanding of biological diversity. Ecological sub-disciplines, particularly conservation, community ecology and macroecology, all recognize the value of evolutionary relationships but the resulting development of phylogenetic approaches has led to a proliferation of phylogenetic diversity metrics. The use of many metrics across the sub-disciplines hampers potential meta-analyses, syntheses, and generalizations of existing results. Further, there is no guide for selecting the appropriate metric for a given question, and different metrics are frequently used to address similar questions. To improve the choice, application, and interpretation of phylo-diversity metrics, we organize existing metrics by expanding on a unifying framework for phylogenetic information. Generally, questions about phylogenetic relationships within or between assemblages tend to ask three types of question: how much; how different; or how regular? We show that these questions reflect three dimensions of a phylogenetic tree: richness, divergence, and regularity. We classify 70 existing phylo-diversity metrics based on their mathematical form within these three dimensions and identify 'anchor' representatives: for α-diversity metrics these are PD (Faith's phylogenetic diversity), MPD (mean pairwise distance), and VPD (variation of pairwise distances). By analysing mathematical formulae and using simulations, we use this framework to identify metrics that mix dimensions, and we provide a guide to choosing and using the most appropriate metrics. We show that metric choice requires connecting the research question with the correct dimension of the framework and that there are logical approaches to selecting and interpreting metrics. The guide outlined herein will help researchers navigate the current jungle of indices.

Basking behavior predicts the evolution of heat tolerance in Australian rainforest lizards.

There is pressing urgency to understand how tropical ectotherms can behaviorally and physiologically respond to climate warming. We examine how basking behavior and thermal environment interact to influence evolutionary variation in thermal physiology of multiple species of lygosomine rainforest skinks from the Wet Tropics of northeastern Queensland, Australia (AWT). These tropical lizards are behaviorally specialized to exploit canopy or sun, and are distributed across marked thermal clines in the AWT. Using phylogenetic analyses, we demonstrate that physiological parameters are either associated with changes in local thermal habitat or to basking behavior, but not both. Cold tolerance, the optimal sprint speed, and performance breadth are primarily influenced by local thermal environment. Specifically, montane lizards are more cool tolerant, have broader performance breadths, and higher optimum sprinting temperatures than their lowland counterparts. Heat tolerance, in contrast, is strongly affected by basking behavior: there are two evolutionary optima, with basking species having considerably higher heat tolerance than shade skinks, with no effect of elevation. These distinct responses among traits indicate the multiple selective pressures and constraints that shape the evolution of thermal performance. We discuss how behavior and physiology interact to shape organisms' vulnerability and potential resilience to climate change.

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.

Phylodiversity to inform conservation policy: An Australian example.

Phylodiversity measures summarise the phylogenetic diversity patterns of groups of organisms. By using branches of the tree of life, rather than its tips (e.g., species), phylodiversity measures provide important additional information about biodiversity that can improve conservation policy and outcomes. As a biodiverse nation with a strong legislative and policy framework, Australia provides an opportunity to use phylogenetic information to inform conservation decision-making. We explored the application of phylodiversity measures across Australia with a focus on two highly biodiverse regions, the south west of Western Australia (SWWA) and the South East Queensland bioregion (SEQ). We analysed seven diverse groups of organisms spanning five separate phyla on the evolutionary tree of life, the plant genera Acacia and Daviesia, mammals, hylid frogs, myobatrachid frogs, passerine birds, and camaenid land snails. We measured species richness, weighted species endemism (WE) and two phylodiversity measures, phylogenetic diversity (PD) and phylogenetic endemism (PE), as well as their respective complementarity scores (a measure of gains and losses) at 20 km resolution. Higher PD was identified within SEQ for all fauna groups, whereas more PD was found in SWWA for both plant groups. PD and PD complementarity were strongly correlated with species richness and species complementarity for most groups but less so for plants. PD and PE were found to complement traditional species-based measures for all groups studied: PD and PE follow similar spatial patterns to richness and WE, but highlighted different areas that would not be identified by conventional species-based biodiversity analyses alone. The application of phylodiversity measures, particularly the novel weighted complementary measures considered here, in conservation can enhance protection of the evolutionary history that contributes to present day biodiversity values of areas. Phylogenetic measures in conservation can include important elements of biodiversity in conservation planning, such as evolutionary potential and feature diversity that will improve decision-making and lead to better biodiversity conservation outcomes.

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.

Assessing biodiversity and endemism using phylogenetic methods across multiple taxonomic groups.

Identifying geographical areas with the greatest representation of the tree of life is an important goal for the management and conservation of biodiversity. While there are methods available for using a single phylogenetic tree to assess spatial patterns of biodiversity, there has been limited exploration of how separate phylogenies from multiple taxonomic groups can be used jointly to map diversity and endemism. Here, we demonstrate how to apply different phylogenetic approaches to assess biodiversity across multiple taxonomic groups. We map spatial patterns of phylogenetic diversity/endemism to identify concordant areas with the greatest representation of biodiversity across multiple taxa and demonstrate the approach by applying it to the Murray-Darling basin region of southeastern Australia. The areas with significant centers of phylogenetic diversity and endemism were distributed differently for the five taxonomic groups studied (plant genera, fish, tree frogs, acacias, and eucalypts); no strong shared patterns across all five groups emerged. However, congruence was apparent between some groups in some parts of the basin. The northern region of the basin emerges from the analysis as a priority area for future conservation initiatives focused on eucalypts and tree frogs. The southern region is particularly important for conservation of the evolutionary heritage of plants and fishes.

Mistaking geography for biology: inferring processes from species distributions.

Over the past few decades, there has been a rapid proliferation of statistical methods that infer evolutionary and ecological processes from data on species distributions. These methods have led to considerable new insights, but they often fail to account for the effects of historical biogeography on present-day species distributions. Because the geography of speciation can lead to patterns of spatial and temporal autocorrelation in the distributions of species within a clade, this can result in misleading inferences about the importance of deterministic processes in generating spatial patterns of biodiversity. In this opinion article, we discuss ways in which patterns of species distributions driven by historical biogeography are often interpreted as evidence of particular evolutionary or ecological processes. We focus on three areas that are especially prone to such misinterpretations: community phylogenetics, environmental niche modelling, and analyses of beta diversity (compositional turnover of biodiversity).

Sharing and re-use of phylogenetic trees (and associated data) to facilitate synthesis.

BACKGROUND: Recently, various evolution-related journals adopted policies to encourage or require archiving of phylogenetic trees and associated data. Such attention to practices that promote sharing of data reflects rapidly improving information technology, and rapidly expanding potential to use this technology to aggregate and link data from previously published research. Nevertheless, little is known about current practices, or best practices, for publishing trees and associated data so as to promote re-use. FINDINGS: Here we summarize results of an ongoing analysis of current practices for archiving phylogenetic trees and associated data, current practices of re-use, and current barriers to re-use. We find that the technical infrastructure is available to support rudimentary archiving, but the frequency of archiving is low. Currently, most phylogenetic knowledge is not easily re-used due to a lack of archiving, lack of awareness of best practices, and lack of community-wide standards for formatting data, naming entities, and annotating data. Most attempts at data re-use seem to end in disappointment. Nevertheless, we find many positive examples of data re-use, particularly those that involve customized species trees generated by grafting to, and pruning from, a much larger tree. CONCLUSIONS: The technologies and practices that facilitate data re-use can catalyze synthetic and integrative research. However, success will require engagement from various stakeholders including individual scientists who produce or consume shareable data, publishers, policy-makers, technology developers and resource-providers. The critical challenges for facilitating re-use of phylogenetic trees and associated data, we suggest, include: a broader commitment to public archiving; more extensive use of globally meaningful identifiers; development of user-friendly technology for annotating, submitting, searching, and retrieving data and their metadata; and development of a minimum reporting standard (MIAPA) indicating which kinds of data and metadata are most important for a re-useable phylogenetic record.