Climate change and land use threaten global hotspots of phylogenetic endemism for trees

Trees are essential for the biosphere and human well-being, providing services like carbon sequestration and habitat provision. However, the majority of tree species are threatened by anthropogenic activities such as habitat loss, overexploitation, and invasions. Range-restricted species (endemics) are at particularly high risk of extinction due to their unique ecological and evolutionary characteristics. Phylogenetic endemism (PE) quantifies the degree to which phylogenetic diversity is concentrated in a specific geographic area, capturing evolutionary rarity and identifying areas of paleoendemism (ancient lineages) and neoendemism (recently diverged lineages). While PE has been studied in some groups, global patterns for tree species remain poorly understood. Previous studies have highlighted the importance of current climate in determining species diversity and endemism; however, past climates also influence speciation, extinction, and dispersal, leaving imprints on PE. Regions with long-term climatic stability may exhibit high PE due to high speciation and low extinction rates. Conversely, regions with pronounced climate oscillations may show neoendemism due to high species turnover. This study addresses the lack of global analysis of tree PE centers by investigating the roles of present and past climate variability in shaping global tree PE patterns and assessing the vulnerability of tree PE hotspots to current and future threats.

The existing literature emphasizes the significant threats to global tree species diversity from anthropogenic activities. Studies have highlighted the vulnerability of range-restricted species, often used to guide conservation prioritization. The concept of phylogenetic endemism (PE) has emerged as a valuable tool to capture evolutionary rarity and inform conservation strategies. While research on PE exists for various taxonomic groups, a comprehensive global assessment of tree PE and its macroecological drivers, particularly considering the interplay of present and past climates, has been lacking. This gap in knowledge has limited our understanding of the vulnerability of tree diversity to future changes.

This study utilized a recently compiled global tree distribution dataset covering 41,835 species (65.1% of known tree species). Phylogenetic endemism (PE) was calculated for each species using a dated phylogenetic tree. The study analyzed the relative roles of present-day climate conditions (annual mean temperature (MAT) and annual precipitation (AP)), and past climate variability (late Miocene and Last Glacial Maximum (LGM)). Paleoclimatic data were used to assess the influence of climate change on PE over geological time scales. Human activity intensity was represented using the Human Modification Index (HMI), integrating 13 different types of human activities. Future climate change impacts were assessed using CMIP6 model projections (SSP370 scenario). The conservation status of PE hotspots was evaluated using existing protected areas data (World Database on Protected Areas, WDPA) and three tree-specific diversity conservation prioritization frameworks (top 17%, 30%, and 50% tree diversity priority areas). Spatial simultaneous autoregressive models (SARs) were used to account for spatial autocorrelation when analyzing the relationship between PE and environmental variables. A two-sample Fisher-Pitman permutation test was used to compare differences between hotspot and non-hotspot regions. Analyses were performed separately for angiosperms and gymnosperms and then compared.

The study revealed that regions with high phylogenetic endemism among tree species are mainly located at low-to-mid latitudes. Angiosperm trees showed distinct spatial PE patterns compared to gymnosperms, with hotspots concentrated in different regions. Approximately 24.3% of angiosperm and 12.0% of gymnosperm distribution grid cells were identified as PE hotspots (neo-, paleo-, and mixed endemism centers). Mixed-endemism centers were the most prevalent type of hotspot for both groups. Analyses using SAR models showed that present-day AP and MAT, along with elevation range, were the strongest predictors of PE for both angiosperm and gymnosperm trees. Paleoclimatic variables (LGM and Miocene MAT and AP anomalies) also significantly influenced PE, suggesting the importance of long-term climate stability. Phylogenetic endemism hotspots exhibited greater elevation ranges, higher MAT and AP, and lower paleoclimatic variability compared to non-hotspot regions. Hotspots were significantly more affected by human pressure (HMI) and projected climate change (future warming and rainfall changes). Existing protected areas offer limited protection for PE hotspots, with gymnosperm-only hotspots entirely unprotected. Implementing the three conservation prioritization frameworks would substantially increase the protection levels for all PE hotspots, with the top 50% priority areas offering near-complete protection.

The findings highlight the crucial role of both current and past climate in shaping global tree PE patterns. The predominance of mixed-endemism centers underscores the importance of long-term environmental stability for maintaining diverse and evolutionarily distinct lineages. The higher human pressure and projected climate change impacts on PE hotspots emphasize the urgency of conservation action. The limited protection offered by existing protected areas necessitates ambitious expansion of protected areas, particularly focusing on the top diversity priority areas. The congruence of PE hotspots identified for trees with those found for other taxonomic groups using the CANAPE approach reinforces the significance of these areas for overall biodiversity and ecosystem functioning. The study's results provide strong evidence for the need to integrate phylogenetic considerations into conservation planning to safeguard evolutionary history and enhance the resilience of tree populations.

This study provides a comprehensive assessment of global tree phylogenetic endemism, identifying key hotspots and their vulnerability to ongoing and future threats. The strong association between PE hotspots and long-term climate stability highlights the potential impact of climate change on tree diversity. The inadequate protection of these hotspots by existing protected areas underscores the need for substantial expansion of protected areas, guided by the prioritized conservation frameworks. Future research should focus on developing and implementing effective conservation strategies for these unique and vulnerable ecosystems, such as assisted colonization or ex-situ conservation, to ensure the long-term persistence of tree diversity and the invaluable ecosystem services they provide.

The study relies on existing species distribution data, which may contain uncertainties and biases, potentially affecting the accuracy of PE estimations. The use of specific CMIP6 models and emission scenarios (SSP370) for future climate projections might not capture the full range of potential climate change impacts. Future research could explore the impacts of other emission scenarios and refine the model projections using more advanced techniques. Also, a 110x110 km resolution might not be fine enough to capture all biodiversity patterns, especially local hotspots.