Phylogenetic patterns of extinction risk in the Eastern Arc Ecosystems, an African biodiversity hotspot

There is an urgent need to reduce drastically the rate at which biodiversity is declining worldwide. Phylogenetic methods are increasingly being recognised as providing a useful framework for predicting future losses, and guiding efforts for preemptive conservation actions. In this study, we used a reconstructed phylogenetic tree of angiosperm species of the Eastern Arc Mountains – an important African biodiversity hotspot – and described the distribution of extinction risk across taxonomic ranks and phylogeny. We provide evidence for both taxonomic and phylogenetic selectivity in extinction risk. However, we found that selectivity varies with IUCN extinction risk category. Vulnerable species are more closely related than expected by chance, whereas endangered and critically endangered species are not significantly clustered on the phylogeny. We suggest that the general observation for taxonomic and phylogenetic selectivity (i.e. phylogenetic signal, the tendency of closely related species to share similar traits) in extinction risks is therefore largely driven by vulnerable species, and not necessarily the most highly threatened. We also used information on altitudinal distribution and climate to generate a predictive model of at-risk species richness, and found that greater threatened species richness is found at higher altitude, allowing for more informed conservation decision making. Our results indicate that evolutionary history can help predict plant susceptibility to extinction threats in the hyper-diverse but woefully-understudied Eastern Arc Mountains, and illustrate the contribution of phylogenetic approaches in conserving African floristic biodiversity where detailed ecological and evolutionary data are often lacking

A global trend towards the loss of evolutionarily unique species in mangrove ecosystems

The mangrove biome stands out as a distinct forest type at the interface between terrestrial, estuarine, and near-shore marine ecosystems. However, mangrove species are increasingly threatened and experiencing range contraction across the globe that requires urgent conservation action. Here, we assess the spatial distribution of mangrove species richness and evolutionary diversity, and evaluate potential predictors of global declines and risk of extinction. We found that human pressure, measured as the number of different uses associated with mangroves, correlated strongly, but negatively, with extinction probability, whereas species ages were the best predictor of global decline, explaining 15% of variation in extinction risk. Although the majority of mangrove species are categorised by the IUCN as Least Concern, our finding that the more threatened species also tend to be those that are more evolutionarily unique is of concern because their extinction would result in a greater loss of phylogenetic diversity. Finally, we identified biogeographic regions that are relatively species-poor but rich in evolutionary history, and suggest these regions deserve greater conservation priority. Our study provides phylogenetic information that is important for developing a unified management plan for mangrove ecosystems worldwide

Marine protected areas are insufficient to conserve global marine plant diversity

AIM : Marine plants are only incidentally included in conservation efforts for marine biodiversity. Here, for the first time, we apply phylogenetic methods to marine macrophytes (mangroves and seagrass species) to test for gaps in the current conservation network by identifying global diversity hotspots for these plant groups, and assess the degree to which hotspots are represented within the current network of marine protected areas (MPAs). LOCATION : Global. METHODS : We calculated five metrics of marine plant diversity: phylogenetic diversity, species richness, species endemism, phylogenetic endemism and ‘evolutionary distinctiveness and global endangerment’ (EDGE). RESULTS : Overall, the diversity of marine plants was poorly represented by current MPAs. Different measures of diversity showed spatial mismatch, demonstrating how strategies that maximize one diversity measure may be inefficient at protecting other facets of marine plant biodiversity. However, complementarity analyses revealed that complete representation can be achieved very efficiently with few additional locations. MAIN CONCLUSIONS : Our study highlights the need for an integrative approach to conserve both the species diversity and phylogenetic diversity of marine plants. While MPAs are a valuable instrument for conserving marine biodiversity, we now face the challenge of increasing coverage to protect other branches of the marine tree of life.http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1466-8238hj2017Plant Production and Soil Scienc

Evidence of constant diversification punctuated by a mass extinction in the African cycads

The recent evidence that extant cycads are not living fossils triggered a renewed search for a better understanding of their evolutionary history. In this study, we investigated the evolutionary diversification history of the genus Encephalartos, a monophyletic cycad endemic to Africa. We found an antisigmoidal pattern with a plateau and punctual explosive radiation. This pattern is typical of a constant radiation with mass extinction. The rate shift that we found may therefore be a result of a rapid recolonization of niches that have been emptied owing to mass extinction. Because the explosive radiation occurred during the transition Pliocene–Pleistocene, we argued that the processes might have been climatically mediated

Unravelling the evolutionary origins of biogeographic assemblages

AIM : Floristic and faunal diversity fall within species assemblages that can be grouped into distinct biomes or ecoregions. Understanding the origins of such biogeographic assemblages helps illuminate the processes shaping present‐day diversity patterns and identifies regions with unique or distinct histories. While the fossil record is often sparse, dated phylogenies can provide a window into the evolutionary past of these regions. Here, we present a novel phylogenetic approach to investigate the evolutionary origins of present‐day biogeographic assemblages and highlight their conservation value. LOCATION : Southern Africa. METHODS : We evaluate the evolutionary turnover separating species clusters in space at different time slices to determine the phylogenetic depth at which the signal for their present‐day structure emerges. We suggest present‐day assemblages with distinct evolutionary histories might represent important units for conservation. We apply our method to the vegetation of southern Africa using a dated phylogeny of the woody flora of the region and explore how the evolutionary history of vegetation types compares to common conservation currencies, including species richness, endemism and threat. RESULTS : We show the differentiation of most present‐day vegetation types can be traced back to evolutionary splits in the Miocene. The woody flora of the Fynbos is the most evolutionarily distinct, and thus has deeper evolutionary roots, whereas the Savanna and Miombo Woodland show close phylogenetic affinities and likely represent a more recent separation. However, evolutionarily distinct phyloregions do not necessarily capture the most unique phylogenetic diversity, nor are they the most species‐rich or threatened. MAIN CONCLUSIONS : Our approach complements analyses of the fossil record and serves as a link to the history of diversification, migration and extinction of lineages within biogeographic assemblages that is separate from patterns of species richness and endemism. Our analysis reveals how phyloregions capture conservation value not represented by traditional biodiversity metrics.The Government of Canada through Genome Canada and Ontario Genomics Institute (2008‐OGI‐ICI‐03), International Development Research Centre (IDRC) and University of Johannesburg.http://wileyonlinelibrary.com/journal/ddi2019-03-01hj2018Plant Production and Soil Scienc

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.The University of Johannesburg, the Royal Society of London, and the National Research Foundation of South Africa. Part of this project was also funded by the Government of Canada through Genome Canada and the Ontario Genomics Institute (2008-OGI-ICI-03).http://www.nrcresearchpress.com/journal/genPlant Scienc

A Global Trend towards the Loss of Evolutionarily Unique Species in Mangrove Ecosystems

Abstract The mangrove biome stands out as a distinct forest type at the interface between terrestrial, estuarine, and near-shore marine ecosystems. However, mangrove species are increasingly threatened and experiencing range contraction across the globe that requires urgent conservation action. Here, we assess the spatial distribution of mangrove species richness and evolutionary diversity, and evaluate potential predictors of global declines and risk of extinction. We found that human pressure, measured as the number of different uses associated with mangroves, correlated strongly, but negatively, with extinction probability, whereas species ages were the best predictor of global decline, explaining 15% of variation in extinction risk. Although the majority of mangrove species are categorised by the IUCN as Least Concern, our finding that the more threatened species also tend to be those that are more evolutionarily unique is of concern because their extinction would result in a greater loss of phylogenetic diversity. Finally, we identified biogeographic regions that are relatively species-poor but rich in evolutionary history, and suggest these regions deserve greater conservation priority. Our study provides phylogenetic information that is important for developing a unified management plan for mangrove ecosystems worldwide

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.APPENDIX S1. Specimen collection frequency across day of flowering year (DOFY), a normalized version of the Julian day of year. Red vertical dashed lines correspond to January 1.APPENDIX S2. Comparison of species peak flowering season (in Julian days) recorded from herbarium specimen records versus the literature (Rebelo, 2001). Rebelo (2001) reports both a “long” season of increased flowering activity and a narrower “short” season of maximal flowering activity for each species, the centers of which are shown here relative to the peak flowering date we calculated from herbarium data as described in the text. Although the y-axis ranges from 0–365, the x-axis has a slightly broader range—given the circular nature of the calendar year, a given Julian date can take multiple values (e.g., 10 = 375), and the value that best communicates alignment with the field guide data set is shown.APPENDIX S3. Parameters used to characterize phenologic responsiveness to climate in Protea species, estimated from the mixed effects model.APPENDIX S4. Changes in flowering times of Protea species across South Africa in relation to anomalies in temperature. Statistical analysis based on mixed effects model using both spatial temperature variation (A) and temporal climate (year-to- year temperature variation) (B) as predictors, with species as random effect. Negative slopes indicate advancement of flowering with warming. Lines indicate fitted slopes for individual Protea species. Points indicate input specimen data, and have been truncated for visualization at the extremes of the y-axis range.APPENDIX S5. Species-specific statistics generated by the sliding window phenology analysis and the mixed effects model (MEM) climate analysis for each of the 25 Protea species.APPENDIX S6. Relationship between the aseasonality of species’ annual flowering phenology cycles (aseasonality index) and their estimated phenological responses to temperature variation across space and time (coefficients from the linear mixed effects model). Dashed lines show linear regressions with 95% confidence intervals shaded.APPENDIX S7. Tests of phylogenetic signal in different dimensions of Protea flowering.Texas A&M University–Corpus Christi, a National Science Foundation Graduate Research Fellowship and the National Science Foundation Postdoctoral Research Fellowship in Biology.http://www.wileyonlinelibrary.com/journal/AppsPlantSciam2020Plant Production and Soil Scienc

Molecular and morphological analysis of subfamily Alooideae (Asphodelaceae) and the inclusion of chortolirion in aloe

Asphodelaceae subfam. Alooideae (Asparagales) currently comprises five genera, four of which are endemic to southern Africa. Despite their importance in commercial horticulture the evolutionary relationships among the genera are still incompletely understood. This study examines phylogenetic relationships in the subfamily using an expanded molecular sequence dataset from three plastid regions (matK, rbcLa, trnH-psbA) and the first subunit of the nuclear ribosomal internal transcribed spacer (ITS1). Sequence data were analysed using maximum parsimony and Bayesian statistics, and selected morphological traits were mapped onto the molecular phylogeny. Haworthia is confirmed as being polyphyletic, comprising three main clades that largely correlate with current subgeneric circumscriptions. Astroloba and Gasteria are evidently each monophyletic and sister respectively to Astroloba and H. subg. Robustipedunculares. Chortolirion is shown to be deeply nested within Aloe and is formally included in that genus. Aloe itself is clearly polyphyletic, with the dwarf species A. aristata allied to Haworthia subg. Robustipedunculares. The taxonomic implications of these findings are examined but branch support at critical lower nodes is insufficient at this stage to justify implementing major taxonomic changes

Spatial overlaps between the global protected areas network and terrestrial hotspots of evolutionary diversity

AIM : A common approach for prioritizing conservation is to identify concentrations (hotspots) of biodiversity. Such hotspots have traditionally been designated on the basis of species‐level metrics (e.g., species richness, endemism and extinction vulnerability). These approaches do not consider phylogenetics explicitly, although phylogenetic relationships reflect the ecological, evolutionary and biogeographical processes by which biodiversity is generated, distributed and maintained. The aim of this study was to identify hotspots of phylogenetic diversity and compare these with hotspots based on species‐level metrics and with the existing protected areas network. LOCATION : Global. TIME PERIOD : Contemporary. MAJOR TAXA STUDIED : Terrestrial vertebrates (mammals, birds and amphibians) and angiosperms. METHODS : We used comprehensive phylogenies and distribution maps of terrestrial birds, mammals, amphibians and angiosperms to identify areas with high concentrations of phylogenetic diversity, phylogenetic endemism, and evolutionary distinctiveness and global endangerment. We compared the locations of these areas with those included within the current network of protected areas and concentrations of species‐level indices: species richness, species endemism and species threat. RESULTS : We found spatial incongruence among the three evolutionary diversity metrics in each taxonomic group. Spatial patterns of diversity and endemism also differed among taxonomic groups, with some differences between vertebrates and angiosperms. Complementarity analyses of phylogenetic diversity identified the minimal area that encapsulates the full branch lengths for each taxonomic group. The current network of protected areas and species‐level hotspots largely does not overlap with areas of high phylodiversity. MAIN CONCLUSION : Overall, < 10% of hotspot areas were designated as protected areas. Patterns of diversity, endemism and vulnerability differ among taxonomic groups.http://wileyonlinelibrary.com/journal/geb2020-06-01hj2019Plant Production and Soil ScienceZoology and Entomolog