Spatial Phylogenetic Analysis of Chinese Lizards: Insights Into Ecological Drivers and Conservation Gaps

Abstract

A major challenge to biodiversity conservation is prioritizing species and regions for conservation under limited resources. Phylogenetic diversity (PD) and phylogenetic endemism (PE) together could provide an effective estimate for biodiversity conservation by identifying areas rich in evolutionarily unique lineages and range-restricted evolutionary history that are in urgent need of protection. Furthermore, understanding the spatial patterns and environmental correlates of these phylogenetic metrices is crucial because it helps to uncover the underlying processes driving biodiversity. We used recently updated distributions and phylogenetic relationships of all Chinese lizards (~90%), and found that the PD and the PE hotspots are mainly located in southern China. We found that temperature plays a stronger role than precipitation, historical climatic stability and seasonality in shaping the spatial patterns of PD and PE. Additionally, PE tends to be higher in regions with greater heterogeneity. Based on the categorical analysis of neo- and paleo-endemism, our results also indicated that the majority of PE hotspots (mix of neo- and paleo-endemism) were located in mountainous terrain (e.g., Hengduan–Himalaya) and on islands (Hainan, Taiwan). Importantly, we show that these hotspots in Chinese mainland are mostly located outside protected areas. Overall, our study highlights these regions with high PD and PE are mainly in mountains of southern and northwestern China. However, current protected areas are insufficient for lizard conservation in China, as they do not adequately cover key centres of evolutionary history.

Keywords

phylogenetic diversity / phylogenetic endemism / protected areas / reptiles / spatial gradients

References

[1] Acevedo, S., and B. Sandel. 2021. “Phylogenetic Endemism Hotspots of North American Birds Are Associated With Warm Temperatures and Long- and Short-Term Climate Stability.” Frontiers in Ecology and Evolution 9: 645396.

[2] Albassatneh, M. C., M. Escudero, A.-C. Monnet, et al. 2021. “Spatial Patterns of Genus- Level Phylogenetic Endemism in the Tree Flora of Mediterranean Europe.” Diversity and Distributions 27: 913–928.

[3] Azevedo, J. A. R., T. B. Guedes, C. D. C. Nogueira, et al. 2020. “Museums and Cradles of Diversity Are Geographically Coincident for Narrowly Distributed Neotropical Snakes.” Ecography 43: 328–339.

[4] Badgley, C., T. M. Smiley, R. Terry, et al. 2017. “Biodiversity and Topographic Complexity: Modern and Geohistorical Perspectives.” Trends in Ecology & Evolution 32: 211–226.

[5] Barratt, C. D., B. A. Bwong, R. E. Onstein, et al. 2017. “Environmental Correlates of Phylogenetic Endemism in Amphibians and the Conservation of Refugia in the Coastal Forests of Eastern Africa.” Diversity and Distributions 23: 875–887.

[6] Bivand, R., G. Millo, and G. Piras. 2021. “A Review of Software for Spatial Econometrics in R.” Mathematics 9: 1276.

[7] Bivand, R. S., E. J. Pebesma, and V. Gomez-Rubio. 2013. spdep: Spatial Dependence: Weighting Schemes, Statistics and Models. R Package. https://CRAN.R-project.org/package=spdep.

[8] Borzée, A.2023. “A 13-step Framework for Better Integration of Streamlined Research.” Integrative Conservation 2: 156–164.

[9] Brodie, J. F., J. Mohd-Azlan, C. Chen, et al. 2023. “Landscape-Scale Benefits of Protected Areas for Tropical Biodiversity.” Nature 620: 807–812.

[10] Cai, B., J. Li, Y. Chen, and Y. Wang. 2016. “Exploring the Status and Causes of China Threatened Reptiles Through the Red List Assessment.” Biodiversity Science 24: 578–587.

[11] Casal-López, M., S. Perea, C. Sousa-Santos, et al. 2018. “Paleobiogeography of an Iberian Endemic Species, Luciobarbus sclateri (Günther, 1868) (Actinopterygii, Cyprinidae), Inferred From Mitochondrial and Nuclear Markers.” Journal of Zoological Systematics and Evolutionary Research 56: 127–147.

[12] Cavender-Bares, J., K. H. Kozak, P. V. Fine, and S. W. Kembel. 2009. “The Merging of Community Ecology and Phylogenetic Biology.” Ecology Letters 12: 693–715.

[13] Coetzee, B. W. T., M. P. Robertson, B. F. N. Erasmus, B. J. V. Rensburg, and W. Thuiller. 2009. “Ensemble Models Predict Important Bird Areas in Southern Africa Will Become Less Effective for Conserving Endemic Birds Under Climate Change.” Global Ecology and Biogeography 18: 701–710.

[14] Cox, N., B. E. Young, P. Bowles, et al. 2022. “A Global Reptile Assessment Highlights Shared Conservation Needs of Tetrapods.” Nature 605: 285–290.

[15] Crisp, M. D., S. Laffan, H. P. Linder, and A. Monro. 2001. “Endemism in the Australian Flora.” Journal of Biogeography 28: 183–198.

[16] D'Amen, M., P. Bombi, P. B. Pearman, D. R. Schmatz, N. E. Zimmermann, and M. A. Bologna. 2011. “Will Climate Change Reduce the Efficacy of Protected Areas for Amphibian Conservation in Italy?” Biological Conservation 144: 989–997.

[17] Daru, B. H., M. V. D. Bank, and T. J. Davies. 2015. “Spatial Incongruence Among Hotspots and Complementary Areas of Tree Diversity in Southern Africa.” Diversity and Distributions 21: 769–780.

[18] Daru, B. H., H. Farooq, A. Antonelli, et al. 2020. “Endemism Patterns Are Scale Dependent.” Nature Communications 11: 2115.

[19] Dormann, C. F., J. M. Mcpherson, M. B. Araújo, et al. 2007. “Methods to Account for Spatial Autocorrelation in the Analysis of Species Distributional Data: A Review.” Ecography 30: 609–628.

[20] Faith, D. P.1992. “Conservation Evaluation and Phylogenetic Diversity.” Biological Conservation 61: 1–10.

[21] Feng, G., Z. Ma, B. Sandel, et al. 2019. “Species and Phylogenetic Endemism in Angiosperm Trees Across the Northern Hemisphere Are Jointly Shaped by Modern Climate and Glacial–Interglacial Climate Change.” Global Ecology and Biogeography 28: 1393–1402.

[22] Ficetola, G. F., M. Falaschi, A. Bonardi, E. Padoa-Schioppa, and R. Sindaco. 2018. “Biogeographical Structure and Endemism Pattern in Reptiles of the Western Palearctic.” Progress in Physical Geography 42: 220–236.

[23] Fick, S. E., and R. J. Hijmans. 2017. “WorldClim 2: New 1-km Spatial Resolution Climate Surfaces for Global Land Areas.” International Journal of Climatology 37: 4302–4315.

[24] Flynn, D. F., N. Mirotchnick, M. Jain, M. I. Palmer, and S. Naeem. 2011. “Functional and Phylogenetic Diversity as Predictors of Biodiversity Ecosystem-Function.” Ecology 92: 1573–1581.

[25] Fritz, S. A., and C. Rahbek. 2012. “Global Patterns of Amphibian Phylogenetic Diversity.” Journal of Biogeography 39: 1373–1382.

[26] Gouveia, S. F., J. Hortal, F. A. S. Cassemiro, T. F. Rangel, and J. A. F. Diniz-Filho. 2013. “Nonstationary Effects of Productivity, Seasonality, and Historical Climate Changes on Global Amphibian Diversity.” Ecography 36: 104–113.

[27] Gumbs, R., C. L. Gray, M. Böhm, et al. 2020. “Global Priorities for Conservation of Reptilian Phylogenetic Diversity in the Face of Human Impacts.” Nature Communications 11: 2616.

[28] Guo, W.-Y., J. M. Serra-Diaz, W. L. Eiserhardt, et al. 2023. “Climate Change and Land Use Threaten Global Hotspots of Phylogenetic Endemism for Trees.” Nature Communications 14: 6950.

[29] Hawkins, B. A., R. Field, H. V. Cornell, et al. 2003. “Energy, Water, and Broad-Scale Geographic Patterns of Species Richness.” Ecology 84: 3105–3117.

[30] Heino, J., J. Alahuhta, and S. Fattorini. 2015. “Phylogenetic Diversity of Regional Beetle Faunas at High Latitudes: Patterns, Drivers and Chance Along Ecological Gradients.” Biodiversity and Conservation 24: 2751–2767.

[31] Hu, Y., H. Fan, Y. Chen, et al. 2021. “Spatial Patterns and Conservation of Genetic and Phylogenetic Diversity of Wildlife in China.” Science Advances 7: eabd5725.

[32] Jetz, W., C. Rahbek, and R. K. Colwell. 2004. “The Coincidence of Rarity and Richness and the Potential Signature of History in Centres of Endemism.” Ecology Letters 7: 1180–1191.

[33] Justin Nowakowski, A., J. I. Watling, A. Murray, et al. 2023. “Protected Areas Slow Declines Unevenly Across the Tetrapod Tree of Life.” Nature 622: 101–106.

[34] Karger, D. N., S. Lange, C. Hari, C. P. O. Reyer, and N. E. Zimmermann. 2021. “CHELSA-W5E5 v1.0: W5E5 v1.0 downscaled With CHELSA v2.0.” ISIMIP Repository.

[35] Keppel, G., K. P. V. Niel, G. W. Wardell-Johnson, et al. 2012. “Refugia: Identifying and Understanding Safe Havens for Biodiversity under Climate Change.” Global Ecology and Biogeography 21: 393–404.

[36] Kougioumoutzis, K., I. P. Kokkoris, M. Panitsa, P. Trigas, A. Strid, and P. Dimopoulos. 2020. “Spatial Phylogenetics, Biogeographical Patterns and Conservation Implications of the Endemic Flora of Crete (Aegean, Greece) Under Climate Change Scenarios.” Biology 9: 199.

[37] Li, W.2004. “The Discovery and Research on Ili Pika (Ochotona iliensis).” Chinese Journal of Zoology 39: 106–111.

[38] Liang, T., and S. Meiri. 2023. “Lizard Richness in Mainland China Is More Strongly Correlated With Energy and Climatic Stability Than With Diversification Rates.” Journal of Biogeography 51: 1–16.

[39] Liang, T., Z. Zhang, W. Y. Dai, L. Shi, and C. H. Lu. 2021. “Spatial Patterns in the Size of Chinese Lizards Are Driven by Multiple Factors.” Ecology and Evolution 11: 9621–9630.

[40] Liang, T., L. Zhou, W. Dai, Z. Zhang, and L. Shi. 2022. “Spatial Patterns and Drivers of Chinese Lizard Richness Among Multiple Scales.” Asian Herpetological Research 13: 117–124.

[41] Lin, L., W. Deng, X. Huang, and B. Kang. 2021. “Fish Taxonomic, Functional, and Phylogenetic Diversity and Their Vulnerabilities in the Largest River in Southeastern China.” Ecology and Evolution 11: 11533–11548.

[42] Mace, G. M., and A. Purvis. 2008. “Evolutionary Biology and Practical Conservation: Bridging a Widening Gap.” Molecular Ecology 17: 9–19.

[43] Mason-Romo, E. D., A. A. Farías, and G. Ceballos. 2017. “Two Decades of Climate Driving the Dynamics of Functional and Taxonomic Diversity of a Tropical Small Mammal Community in Western Mexico.” PLoS One 12: 0189104.

[44] Maxwell, S. L., V. Cazalis, N. Dudley, et al. 2020. “Area-Based Conservation in the Twenty-First Century.” Nature 586: 217–227.

[45] Mi, C., X. Han, Z. Jiang, Z. Zeng, W. Du, and B. Sun. 2024. “Precipitation and Temperature Primarily Determine the Reptile Distributions in China.” Ecography 2024: e07005.

[46] Mishler, B. D.2023. “Spatial Phylogenetics.” Journal of Biogeography 50: 1454–1463.

[47] Mishler, B. D., N. Knerr, C. E. González-Orozco, A. H. Thornhill, S. W. Laffan, and J. T. Miller. 2014. “Phylogenetic Measures of Biodiversity and Neo- and Paleo-Endemism in Australian Acacia.” Nature Communications 5: 4473.

[48] Mouillot, D., V. Parravicini, D. R. Bellwood, et al. 2016. “Global Marine Protected Areas Do Not Secure the Evolutionary History of Tropical Corals and Fishes.” Nature Communications 7: 10359.

[49] Murali, G., R. Gumbs, S. Meiri, and U. Roll. 2021. “Global Determinants and Conservation of Evolutionary and Geographic Rarity in Land Vertebrates.” Science Advances 7: 5582.

[50] Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. A. da Fonseca, and J. Kent. 2000. “Biodiversity Hotspots for Conservation Priorities.” Nature 403: 853–858.

[51] Nekola, J.1999. “Paleorefugia and Neorefugia: The Influence of Colonization History on Community Pattern and Process.” Ecology 80: 2459–2473.

[52] Nitta, J. H., B. D. Mishler, W. Iwasaki, and A. Ebihara. 2022. “Spatial Phylogenetics of Japanese Ferns: Patterns, Processes, and Implications for Conservation.” Botany 109: 727–745.

[53] Ohlemüller, R., B. J. Anderson, M. B. Araújo, et al. 2008. “The Coincidence of Climatic and Species Rarity: High Risk to Small-Range Species From Climate Change.” Biology Letters 4: 568–572.

[54] Paúl, M. J., D. Rosauer, P. Tarroso, G. Velo-Antón, and S. B. Carvalho. 2023. “Environmental and Topographic Drivers of Amphibian Phylogenetic Diversity and Endemism in the Iberian Peninsula.” Ecology and Evolution 13: e9666.

[55] Paz, A., J. L. Brown, C. L. O. Cordeiro, et al. 2021. “Environmental Correlates of Taxonomic and Phylogenetic Diversity in the Atlantic Forest.” Journal of Biogeography 48: 1377–1391.

[56] Pepper, M., M. K. Fujita, C. Moritz, and J. S. Keogh. 2011. “Palaeoclimate Change Drove Diversification Among Isolated Mountain Refugia in the Australian Arid Zone.” Molecular Ecology 20: 1529–1545.

[57] R Core Team. 2023. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing.

[58] Rahbek, C., M. K. Borregaard, A. Antonelli, et al. 2019. “Building Mountain Biodiversity: Geological and Evolutionary Processes.” Science 365: 1114–1119.

[59] Roll, U., A. Feldman, and M. Novosolov, et al., TRAP. 2017. “The Global Distribution of Tetrapods Reveals a Need for Targeted Reptile Conservation.” Nature Ecology & Evolution 1: 1677–1682.

[60] Rosauer, D., S. W. Laffan, M. D. Crisp, S. C. Donnellan, and L. G. Cook. 2009. “Phylogenetic Endemism: A New Approach for Identifying Geographical Concentrations of Evolutionary History.” Molecular Ecology 18: 4061–4072.

[61] Rosauer, D. F., and W. Jetz. 2015. “Phylogenetic Endemism in Terrestrial Mammals.” Global Ecology & Biogeography 24: 168–179.

[62] Saha, A., L. Mcrae, C. K. Dodd, et al. 2018. “Tracking Global Population Trends: Population Time-Series Data and a Living Planet Index for Reptiles.” Journal of Herpetology 52 no. 3: 259–268.

[63] Sandel, B., P. Weigelt, H. Kreft, et al. 2020. “Current Climate, Isolation and History Drive Global Patterns of Tree Phylogenetic Endemism.” Global Ecology and Biogeography 29: 4–15.

[64] Silva, F. R. D., M. Almeida-Neto, V. H. M. D. Prado, C. F. B. Haddad, and D. D. C. Rossa-Feres. 2012. “Humidity Levels Drive Reproductive Modes and Phylogenetic Diversity of Amphibians in the Brazilian Atlantic Forest.” Journal of Biogeography, 39: 1720–1732.

[65] Stebbins, G. L., and J. Major. 1965. “Endemism and Speciation in the California Flora.” Ecological Monographs 35: 1–35.

[66] Stevens, G. C.1989. “The Latitudinal Gradient in Geographical Range: How so Many Species Coexist in the Tropics.” American Naturalist 133: 240–256.

[67] Thuiller, W., D. Gravel, G. F. Ficetola, et al. 2020. “Productivity Begets Less Phylogenetic Diversity but Higher Uniqueness Than Expected.” Journal of Biogeography 47: 44–58.

[68] Title, P. O., D. L. Swiderski, and M. L. Zelditch. 2022. “EcoPhyloMapper: An r Package for Integrating Geographical Ranges, Phylogeny and Morphology.” Methods in Ecology and Evolution 13: 1912–1922.

[69] Toro-Núñez, O., and A. Lira-Noriega. 2020. “Discordant Phylogenetic Endemism Patterns in a Recently Diversified Brassicaceae Lineage From the Atacama Desert: When Choices in Phylogenetics and Species Distribution Information Matter.” Journal of Biogeography 47: 1792–1804.

[70] Trigas, P., M. Panitsa, and S. Tsiftsis. 2013. “Elevational Gradient of Vascular Plant Species Richness and Endemism in Crete—The Effect of Post-Isolation Mountain Uplift on a Continental Island System.” PLoS One 8: 59425.

[71] Tucker, C. M., T. Aze, M. W. Cadotte, et al. 2019. “Assessing the Utility of Conserving Evolutionary History.” Biological Reviews of the Cambridge Philosophical Society 94: 1740–1760.

[72] Uetz, P., P. Freed, R. Aguilar, F. Reyes, J. Kudera, and J. Hošek. 2024. “The Reptile Database.” Accessed March 1, 2024. http://www.reptile-database.org.

[73] UNEP-WCMC & IUCN. 2023. “Protected Planet: The World Database on Protected Areas (WDPA) and World Database on Other Effective Area-Based Conservation Measures (WD-OECM), October 2023.” UNEP-WCMC and IUCN. www.protectedplanet.net.

[74] Varzinczak, L. H., T. B. Zanata, M. O. Moura, and F. C. Passos. 2020. “Geographical Patterns and Current and Short-Term Historical Correlates of Phylogenetic Diversity and Endemism for New World Primates.” Journal of Biogeography 47: 890–902.

[75] Venter, O., E. W. Sanderson, A. Magrach, et al. 2016. “Sixteen Years of Change in the Global Terrestrial Human Footprint and Implications for Biodiversity Conservation.” Nature Communications 7: 12558.

[76] Vicente, G., and T. Wilfried. 2020. “Farmland Bird Assemblages Exhibit Higher Functional and Phylogenetic Diversity Than Forest Assemblages in France.” Journal of Biogeography 47, no. 11: 2392–2404.

[77] Voskamp, A., D. J. Baker, P. A. Stephens, P. J. Valdes, and S. G. Willis. 2017. “Global Patterns in the Divergence Between Phylogenetic Diversity and Species Richness in Terrestrial Birds.” Journal of Biogeography 44: 709–721.

[78] Wang, K., J. L. Ren, H. M. Chen, et al. 2020. “The Updated Checklists of Amphibians and Reptiles of China.” Biodiversity Science 28: 189–218.

[79] Wang, K., Y. Wu, and Z. Yuan. 2021. “China's New Laws Overlook Native Herpetofauna.” Science 371, no. 6533: 1002–1003.

[80] Wauchope, H. S., J. Jones, J. Geldmann, et al. 2022. “Protected Areas Have a Mixed Impact on Waterbirds, but Management Helps.” Nature 605: 103–107.

[81] Webb, C. O., D. D. Ackerly, M. A. Mcpeek, and M. J. Donoghue. 2002. “Phylogenies and Community Ecology.” Annual Review of Ecology and Systematics 33: 475–505.

[82] Wu, Z., A. Borzée, T. Qian, W. Dai, S. Li, and J. Wang. 2023. “Spatial Non-Stationarity Effect of Determinants Regulates Variation in Amphibian Species Richness.” Ecological Indicators 150: 110268.

[83] Xu, W., Y.-H. Wu, W.-W. Zhou, et al. 2024. “Hidden Hotspots of Amphibian Biodiversity in China.” Proceedings of the National Academy of Sciences of the United States of America 121: e2320674121.

[84] Zhong, Y., C. Chen, and Y. Wang. 2022. “Biological and Extrinsic Correlates of Extinction Risk in Chinese Lizards.” Current Zoology 68: 285–293.

RIGHTS & PERMISSIONS

2025 The Author(s). Integrative Conservation published by John Wiley & Sons Australia, Ltd on behalf of Xishuangbanna Tropical Botanical Garden (XTBG).