Indicators to monitor the status of the tree of life.

Following the failure to fully achieve any of the 20 Aichi biodiversity targets, the future of biodiversity rests in the balance. The Convention on Biological Diversity's Kunming-Montreal Global Biodiversity Framework (GBF) presents the opportunity to preserve nature's contributions to people (NCPs) for current and future generations by conserving biodiversity and averting extinctions. There is a need to safeguard the tree of life-the unique and shared evolutionary history of life on Earth-to maintain the benefits it bestows into the future. Two indicators have been adopted within the GBF to monitor progress toward safeguarding the tree of life: the phylogenetic diversity (PD) indicator and the evolutionarily distinct and globally endangered (EDGE) index. We applied both to the world's mammals, birds, and cycads to show their utility at the global and national scale. The PD indicator can be used to monitor the overall conservation status of large parts of the evolutionary tree of life, a measure of biodiversity's capacity to maintain NCPs for future generations. The EDGE index is used to monitor the performance of efforts to conserve the most distinctive species. The risk to PD of birds, cycads, and mammals increased, and mammals exhibited the greatest relative increase in threatened PD over time. These trends appeared robust to the choice of extinction risk weighting. EDGE species had predominantly worsening extinction risk. A greater proportion of EDGE mammals (12%) had increased extinction risk compared with threatened mammals in general (7%). By strengthening commitments to safeguarding the tree of life, biodiversity loss can be reduced and thus nature's capacity to provide benefits to humanity now and in the future can be preserved.

Indicadores para monitorear el estado del árbol de la vida Resumen El futuro de la biodiversidad peligra tras no haberse logrado ninguno de los 20 Objetivos de Aichi. El Marco Global de Biodiversidad (GBF) de Kunming-Montreal del Convenio sobre la Diversidad Biológica (CDB) representa la oportunidad de preservar las contribuciones de la naturaleza a las personas (PNC) para las generaciones actuales y futuras mediante la conservación de la biodiversidad y la prevención de las extinciones. Es necesario salvaguardar el árbol de la vida -la historia evolutiva única y compartida de la vida en la Tierra- para mantener en el futuro los beneficios que aporta. En el GBF se han adoptado dos indicadores para supervisar los avances hacia el cuidado del árbol de la vida: el indicador de diversidad filogenética y el índice de especies evolutivamente distintas y globalmente amenazadas (EDGE). Aplicamos ambos a los mamíferos, las aves y las cícadas del mundo para demostrar su utilidad a escala mundial y nacional. El indicador de diversidad filogenética puede utilizarse para supervisar el estado de conservación general de grandes partes del árbol evolutivo de la vida, una medida de la capacidad de la biodiversidad para mantener los PNC para las generaciones futuras. El índice EDGE se utiliza para supervisar el rendimiento de los esfuerzos por conservar las especies más distintivas. El riesgo para la diversidad filogenética de aves, cícadas y mamíferos aumentó, y los mamíferos mostraron el mayor aumento relativo de la diversidad filogenética amenazada a lo largo del tiempo. Estas tendencias parecieron sólidas a la hora de elegir la valoración del riesgo de extinción. Las especies EDGE tuvieron un riesgo de extinción predominante cada vez peor. Una mayor proporción de mamíferos EDGE (12%) presentó un riesgo de extinción creciente en comparación con los mamíferos amenazados en general (7%). Si se refuerza el compromiso de salvaguardar el árbol de la vida, se puede reducir la pérdida de biodiversidad y preservar así la capacidad de la naturaleza para proporcionar beneficios a la humanidad ahora y en el futuro.

Reorganization of seagrass communities in a changing climate.

Although climate change projections indicate significant threats to terrestrial biodiversity, the effects are much more profound and striking in the marine environment. Here we explore how different facets of locally distinctive α- and ß-diversity (changes in spatial composition) of seagrasses will respond to future climate change scenarios across the globe and compare their coverage with the existing network of marine protected areas. By using species distribution modelling and a dated phylogeny, we predict widespread reductions in species' range sizes that will result in increases in seagrass weighted and phylogenetic endemism. These projected increases of endemism will result in divergent shifts in the spatial composition of ß-diversity leading to differentiation in some areas and the homogenization of seagrass communities in other regions. Regardless of the climate scenario, the potential hotspots of these projected shifts in seagrass α- and ß-diversity are predicted to occur outside the current network of marine protected areas, providing new priority areas for future conservation planning that incorporate seagrasses. Our findings report responses of species to future climate for a group that is currently under represented in climate change assessments yet crucial in maintaining marine food chains and providing habitat for a wide range of marine biodiversity.

Mass production of unvouchered records fails to represent global biodiversity patterns.

The ever-increasing human footprint even in very remote places on Earth has inspired efforts to document biodiversity vigorously in case organisms go extinct. However, the data commonly gathered come from either primary voucher specimens in a natural history collection or from direct field observations that are not traceable to tangible material in a museum or herbarium. Although both datasets are crucial for assessing how anthropogenic drivers affect biodiversity, they have widespread coverage gaps and biases that may render them inefficient in representing patterns of biodiversity. Using a large global dataset of around 1.9 billion occurrence records of terrestrial plants, butterflies, amphibians, birds, reptiles and mammals, we quantify coverage and biases of expected biodiversity patterns by voucher and observation records. We show that the mass production of observation records does not lead to higher coverage of expected biodiversity patterns but is disproportionately biased toward certain regions, clades, functional traits and time periods. Such coverage patterns are driven by the ease of accessibility to air and ground transportation, level of security and extent of human modification at each sampling site. Conversely, voucher records are vastly infrequent in occurrence data but in the few places where they are sampled, showed relative congruence with expected biodiversity patterns for all dimensions. The differences in coverage and bias by voucher and observation records have important implications on the utility of these records for research in ecology, evolution and conservation research.

Widespread homogenization of plant communities in the Anthropocene.

Native biodiversity decline and non-native species spread are major features of the Anthropocene. Both processes can drive biotic homogenization by reducing trait and phylogenetic differences in species assemblages between regions, thus diminishing the regional distinctiveness of biotas and likely have negative impacts on key ecosystem functions. However, a global assessment of this phenomenon is lacking. Here, using a dataset of >200,000 plant species, we demonstrate widespread and temporal decreases in species and phylogenetic turnover across grain sizes and spatial extents. The extent of homogenization within major biomes is pronounced and is overwhelmingly explained by non-native species naturalizations. Asia and North America are major sources of non-native species; however, the species they export tend to be phylogenetically close to recipient floras. Australia, the Pacific and Europe, in contrast, contribute fewer species to the global pool of non-natives, but represent a disproportionate amount of phylogenetic diversity. The timeline of most naturalisations coincides with widespread human migration within the last ~500 years, and demonstrates the profound influence humans exert on regional biotas beyond changes in species richness.

Bias assessments to expand research harnessing biological collections.

Biological collections are arguably the most important resources for investigations into the impacts of human activities on biodiversity. However, the apparent opportunities presented by museum-derived datasets have not resulted in consistent or widespread use of specimens in ecology outside phenological research and species distribution modeling. We attribute this gap between opportunity and application to biases introduced by collectors, curators, and preservation practices and an imperfect understanding of these biases and how to mitigate them. To facilitate broader use of specimen-based data, we characterize collection biases across key axes and explore interactions among them. We then present a framework for determining the bias assessments needed when extracting data from biological collections. We show that bias assessments required by particular ecological studies will depend on the response variables being measured and the predictor axes of interest. We argue that quantification of biases in specimen-derived datasets is needed to facilitate the widespread application of these data.

Exploring a new way to think about climate regions.

A new system for classifying climates emerges from modeling the environmental conditions that 26,000 species of tetrapods experience in their home range.

Savanna tree evolutionary ages inform the reconstruction of the paleoenvironment of our hominin ancestors.

Ideas on hominin evolution have long invoked the emergence from forests into open habitats as generating selection for traits such as bipedalism and dietary shifts. Though controversial, the savanna hypothesis continues to motivate research into the palaeo-environments of Africa. Reconstruction of these ancient environments has depended heavily on carbon isotopic analysis of fossil bones and palaeosols. The sparsity of the fossil record, however, imposes a limit to the strength of inference that can be drawn from such data. Time-calibrated phylogenies offer an additional tool for dating the spread of savanna habitat. Here, using the evolutionary ages of African savanna trees, we suggest an initial tropical or subtropical expansion of savanna between 10 and 15 Ma, which then extended to higher latitudes, reaching southern Africa ca. 3 Ma. Our phylogenetic estimates of the origin and latitudinal spread of savannas broadly correspond with isotopic age estimates and encompass the entire hominin fossil record. Our results are consistent with the savanna hypothesis of early hominin evolution and reignite the debate on the drivers of savanna expansion. Our analysis demonstrates the utility of phylogenetic proxies for dating major ecological transitions in geological time, especially in regions where fossils are rare or absent or occur in discontinuous sediments.

Endemism patterns are scale dependent.

Areas of endemism are important in biogeography because they capture facets of biodiversity not represented elsewhere. However, the scales at which they are relevant to research and conservation are poorly analysed. Here, we calculate weighted endemism (WE) and phylogenetic endemism (PE) separately for all birds and amphibians across the globe. We show that scale dependence is widespread for both indices and manifests across grain sizes, spatial extents and taxonomic treatments. Variations in taxonomic opinions-whether species are treated by systematic 'lumping' or 'splitting'-can profoundly affect the allocation of WE hotspots. Global patterns of PE can provide insights into complex evolutionary processes but this congruence is lost at the continental to country extents. These findings are explained by environmental heterogeneity at coarser grains, and to a far lesser extent at finer resolutions. Regardless of scale, we find widespread deficits of protection for endemism hotspots. Our study presents a framework for assessing areas for conservation that are robust to assumptions on taxonomy, spatial grain and extent.

Temperature controls phenology in continuously flowering Protea species of subtropical Africa.

PREMISE OF THE STUDY: Herbarium specimens are increasingly used as records of plant flowering phenology. However, most herbarium-based studies on plant phenology focus on taxa from temperate regions. Here, we explore flowering phenologic responses to climate in the subtropical plant genus Protea (Proteaceae), an iconic group of plants that flower year-round and are endemic to subtropical Africa. METHODS: We present a novel, circular sliding window approach to investigate phenological patterns developed for species with year-round flowering. We employ our method to evaluate the extent to which site-to-site and year-to-year variation in temperature and precipitation affect flowering dates using a database of 1727 herbarium records of 25 Protea species. We also explore phylogenetic conservatism in flowering phenology. RESULTS: We show that herbarium data combined with our sliding window approach successfully captured independently reported flowering phenology patterns (r = 0.93). Both warmer sites and warmer years were associated with earlier flowering of 3-5 days/°C, whereas precipitation variation had no significant effect on flowering phenology. Although species vary widely in phenological responsiveness, responses are phylogenetically conserved, with closely related species tending to shift flowering similarly with increasing temperature. DISCUSSION: Our results point to climate-responsive phenology for this important plant genus and indicate that the subtropical, aseasonally flowering genus Protea has temperature-driven flowering responses that are remarkably similar to those of better-studied northern temperate plant species, suggesting a generality across biomes that has not been described elsewhere.

Biological collections for understanding biodiversity in the Anthropocene.

Global change has become a central focus of modern biology. Yet, our knowledge of how anthropogenic drivers affect biodiversity and natural resources is limited by a lack of biological data spanning the Anthropocene. We propose that the hundreds of millions of plant, fungal and animal specimens deposited in natural history museums have the potential to transform the field of global change biology. We suggest that museum specimens are underused, particularly in ecological studies, given their capacity to reveal patterns that are not observable from other data sources. Increasingly, museum specimens are becoming mobilized online, providing unparalleled access to physiological, ecological and evolutionary data spanning decades and sometimes centuries. Here, we describe the diversity of collections data archived in museums and provide an overview of the diverse uses and applications of these data as discussed in the accompanying collection of papers within this theme issue. As these unparalleled resources are under threat owing to budget cuts and other institutional pressures, we aim to shed light on the unique discoveries that are possible in museums and, thus, the singular value of natural history collections in a period of rapid change.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

A novel proof of concept for capturing the diversity of endophytic fungi preserved in herbarium specimens.

Herbarium specimens represent important records of morphological and genetic diversity of plants that inform questions relevant to global change, including species distributions, phenology and functional traits. It is increasingly appreciated that plant microbiomes can influence these aspects of plant biology, but little is known regarding the historic distribution of microbes associated with plants collected in the pre-molecular age. If microbiomes can be observed reliably in herbarium specimens, researchers will gain a new lens with which to examine microbial ecology, evolution, species interactions. Here, we describe a method for accessing historical plant microbiomes from preserved herbarium specimens, providing a proof of concept using two plant taxa from the imperiled boreal biome (Andromeda polifolia and Ledum palustre subsp. groenlandicum, Ericaceae). We focus on fungal endophytes, which occur within symptomless plant tissues such as leaves. Through a three-part approach (i.e. culturing, cloning and next-generation amplicon sequencing via the Illumina MiSeq platform, with extensive controls), we examined endophyte communities in dried, pressed leaves that had been processed as regular herbarium specimens and stored at room temperature in a herbarium for four years. We retrieved only one endophyte in culture, but cloning and especially the MiSeq analysis revealed a rich community of foliar endophytes. The phylogenetic distribution and diversity of endophyte assemblages, especially among the Ascomycota, resemble endophyte communities from fresh plants collected in the boreal biome. We could distinguish communities of endophytes in each plant species and differentiate likely endophytes from fungi that could be surface contaminants. Taxa found by cloning were observed in the larger MiSeq dataset, but species richness was greater when subsets of the same tissues were evaluated with the MiSeq approach. Our findings provide a proof of concept for capturing endophyte DNA from herbarium specimens, supporting the importance of herbarium records as roadmaps for understanding the dynamics of plant-associated microbial biodiversity in the Anthropocene.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Widespread sampling biases in herbaria revealed from large-scale digitization.

Nonrandom collecting practices may bias conclusions drawn from analyses of herbarium records. Recent efforts to fully digitize and mobilize regional floras online offer a timely opportunity to assess commonalities and differences in herbarium sampling biases. We determined spatial, temporal, trait, phylogenetic, and collector biases in c. 5 million herbarium records, representing three of the most complete digitized floras of the world: Australia (AU), South Africa (SA), and New England, USA (NE). We identified numerous shared and unique biases among these regions. Shared biases included specimens collected close to roads and herbaria; specimens collected more frequently during biological spring and summer; specimens of threatened species collected less frequently; and specimens of close relatives collected in similar numbers. Regional differences included overrepresentation of graminoids in SA and AU and of annuals in AU; and peak collection during the 1910s in NE, 1980s in SA, and 1990s in AU. Finally, in all regions, a disproportionately large percentage of specimens were collected by very few individuals. We hypothesize that these mega-collectors, with their associated preferences and idiosyncrasies, shaped patterns of collection bias via 'founder effects'. Studies using herbarium collections should account for sampling biases, and future collecting efforts should avoid compounding these biases to the extent possible.

Understanding the Processes Underpinning Patterns of Phylogenetic Regionalization.

A key step in understanding the distribution of biodiversity is the grouping of regions based on their shared elements. Historically, regionalization schemes have been largely species centric. Recently, there has been interest in incorporating phylogenetic information into regionalization schemes. Phylogenetic regionalization can provide novel insights into the mechanisms that generate, distribute, and maintain biodiversity. We argue that four processes (dispersal limitation, extinction, speciation, and niche conservatism) underlie the formation of species assemblages into phylogenetically distinct biogeographic units. We outline how it can be possible to distinguish among these processes, and identify centers of evolutionary radiation, museums of diversity, and extinction hotspots. We suggest that phylogenetic regionalization provides a rigorous and objective classification of regional diversity and enhances our knowledge of biodiversity patterns.

Integrating biogeography, threat and evolutionary data to explore extinction crisis in the taxonomic group of cycads.

Will the ongoing extinction crisis cause a severe loss of evolutionary information accumulated over millions of years on the tree of life? This question has been largely explored, particularly for vertebrates and angiosperms. However, no equivalent effort has been devoted to gymnosperms. Here, we address this question focusing on cycads, the gymnosperm group exhibiting the highest proportion of threatened species in the plant kingdom. We assembled the first complete phylogeny of cycads and assessed how species loss under three scenarios would impact the cycad tree of life. These scenarios are as follows: (1) All top 50% of evolutionarily distinct (ED) species are lost; (2) all threatened species are lost; and (3) only all threatened species in each IUCN category are lost. Finally, we analyzed the biogeographical pattern of cycad diversity hotspots and tested for gaps in the current global conservation network. First, we showed that threatened species are not significantly clustered on the cycad tree of life. Second, we showed that the loss of all vulnerable or endangered species does not depart significantly from random loss. In contrast, the loss of all top 50% ED, all threatened or all critically endangered species, would result in a greater loss of PD (Phylogenetic Diversity) than expected. To inform conservation decisions, we defined five hotpots of diversity, and depending on the diversity metric used, these hotspots are located in Southern Africa, Australia, Indo-Pacific, and Mexico and all are found within protected areas. We conclude that the phylogenetic diversity accumulated over millions of years in the cycad tree of life would not survive the current extinction crisis. As such, prioritizing efforts based on ED and concentrating efforts on critically endangered species particularly in southern Africa, Australia, Indo-Pacific, and Mexico are required to safeguarding the evolutionary diversity in the cycad tree of life.

Testing the reliability of standard and complementary DNA barcodes for the monocot subfamily Alooideae from South Africa.

Although a standard DNA barcode has been identified for plants, it does not always provide species-level specimen identifications for investigating important ecological questions. In this study, we assessed the species-level discriminatory power of standard (rbcLa + matK) and complementary barcodes (ITS1 and trnH-psbA) within the subfamily Alooideae (Asphodelaceae), a large and recent plant radiation, whose species are important in horticulture yet are threatened. Alooideae has its centre of endemism in southern Africa, with some outlier species occurring elsewhere in Africa and Madagascar. We sampled 360 specimens representing 235 species within all 11 genera of the subfamily. With three distance-based methods, all markers performed poorly for our combined data set, with the highest proportion of correct species-level specimen identifications (30%) found for ITS1. However, when performance was assessed across genera, the discriminatory power varied from 0% for all single markers and combinations in Gasteria to 63% in Haworthiopsis, again for ITS1, suggesting that DNA barcoding success may be related to the evolutionary history of the lineage considered. Although ITS1 could be a good barcode for Haworthiopsis, the generally poor performance of all markers suggests that Alooideae remains a challenge. As species boundaries within Alooideae remain controversial, we call for continued search for suitable markers or the use of genomics approaches to further explore species discrimination in the group.

Spiny plants, mammal browsers, and the origin of African savannas.

Savannas first began to spread across Africa during the Miocene. A major hypothesis for explaining this vegetation change is the increase in C4 grasses, promoting fire. We investigated whether mammals could also have contributed to savanna expansion by using spinescence as a marker of mammal herbivory. Looking at the present distribution of 1,852 tree species, we established that spinescence is mainly associated with two functional types of mammals: large browsers and medium-sized mixed feeders. Using a dated phylogeny for the same tree species, we found that spinescence evolved at least 55 times. The diversification of spiny plants occurred long after the evolution of Afrotherian proboscideans and hyracoids. However, it is remarkably congruent with diversification of bovids, the lineage including the antelope that predominantly browse these plants today. Our findings suggest that herbivore-adapted savannas evolved several million years before fire-maintained savannas and probably, in different environmental conditions. Spiny savannas with abundant mammal herbivores occur in drier climates and on nutrient-rich soils, whereas fire-maintained savannas occur in wetter climates on nutrient-poor soils.

DNA barcodes reveal microevolutionary signals in fire response trait in two legume genera.

Large-scale DNA barcoding provides a new technique for species identification and evaluation of relationships across various levels (populations and species) and may reveal fundamental processes in recently diverged species. Here, we analysed DNA sequence variation in the recently diverged legumes from the Psoraleeae (Fabaceae) occurring in the Cape Floristic Region (CFR) of southern Africa to test the utility of DNA barcodes in species identification and discrimination. We further explored the phylogenetic signal on fire response trait (reseeding and resprouting) at species and generic levels. We showed that Psoraleoid legumes of the CFR exhibit a barcoding gap yielding the combination of matK and rbcLa (matK + rbcLa) data set as a better barcode than single regions. We found a high score (100 %) of correct identification of individuals to their respective genera but a very low score (<50 %) in identifying them to species. We found a considerable match (54 %) between genetic species and morphologically delimited species. We also found that different lineages showed a weak but significant phylogenetic conservatism in their response to fire as reseeders or resprouters, with more clustering of resprouters than would be expected by chance. These novel microevolutionary patterns might be acting continuously over time to produce multi-scale regularities of biodiversity. This study provides the first insight into the DNA barcoding campaign of land plants in species identification and detection of the phylogenetic signal in recently diverged lineages of the CFR.