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Phylogenetic Dispersion and Diversity in Regional Assemblages of Seed Plants in China

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Phylogenetic Dispersion and Diversity in Regional Assemblages of Seed Plants in China Phylogenetic dispersion and diversity in regional assemblages of seed plants in China Hong Qiana,b,1,2, Tao Denga,1, Yi Jinc,1, Lingfeng Maod, Dan Zhaoe, and Robert E. Ricklefsf,2 aCAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; bResearch and Collections Center, Illinois State Museum, Springfield, IL 62703; cState Key Laboratory of Plant Physiology and Development in Guizhou Province, School of Life Sciences, Guizhou Normal University, Guiyang 550001, China; dCo-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China; eInstitute of Ecological Resources and Landscape Architecture, Chengdu University of Technology, Chengdu 610059, China; and fDepartment of Biology, University of Missouri–St. Louis, St. Louis, MO 63121 Contributed by Robert E. Ricklefs, June 20, 2019 (sent for review January 2, 2019; reviewed by Zhiyao Tang and Yaowu Xing) Species assemble into communities through ecological and evolu- ronmental filtering than communities in less stressful conditions. tionary processes. Phylogenetic niche conservatism—the tendency Thus, communities in more stressful environments should exhibit of species to retain ancestral ecological distributions—is thought higher phylogenetic relatedness (clustering) and lower phylogenetic to influence which species from a regional species pool can persist diversity. in a particular environment. We analyzed data for seed plants in Most of the major clades of present-day organisms first China to test hypotheses about the distribution of species within appeared when our planet was dominated by tropical environ- regional floras. Of 16 environmental variables, actual evapotrans- ments (10, 11). For example, many taxonomic families of seed piration, minimum temperature of the coldest month, and annual plants originated during the warm period between the beginning precipitation most strongly influenced regional species richness, of the Cretaceous and the end of the Eocene (12), when global phylogenetic dispersion, and phylogenetic diversity for both climate cooling (13) forced clades of warm-adapted plants at gymnosperms (cone-bearing plants) and angiosperms (flowering higher latitudes to retreat to lower latitudes, evolve tolerance of plants). For most evolutionary clades at, and above, the family colder temperatures, or become extinct. Because ecological traits level, the relationships between metrics of phylogenetic dispersion tend to be phylogenetically conserved (1, 6, 7), few members of (i.e., average phylogenetic distance among species), or phylogenetic clades cross major ecophysiological boundaries, particularly to- diversity, and the 3 environmental variables were consistent with ward harsher (e.g., colder) environments (14). Thus, most trop- the tropical niche conservatism hypothesis, which predicts closer ical clades fail to disperse into extratropical regions because they phylogenetic relatedness and reduced phylogenetic diversity with lack ecological and physiological adaptations to survive winter increasing environmental stress. The slopes of the relationships be- temperatures below freezing (15, 16). Accordingly, species in tween phylogenetic relatedness and the 3 environmental drivers regions with colder and drier (i.e., more stressful) climates identified in this analysis were steeper for primarily tropical clades, should be more closely related phylogenetically (clustered) due implying greater niche conservatism, than for primarily temperate to PNC. This expectation is often referred to as the “tropical clades. These observations suggest that the distributions of seed niche conservatism” hypothesis because adaptations to tolerate plants across large-scale environmental gradients in China are con- freezing conditions rarely evolve in tropical clades (6, 7). strained by conserved adaptations to the physical environment, i.e., phylogenetic niche conservatism. Significance environmental filtering | niche conservatism | phylogenetic diversity | phylogenetic relatedness | seed plants Ecological and evolutionary processes work together in the assembly of regional and local communities from available he presence of a species in a local ecological assemblage, or species pools based on species traits linked to ecological tol- Tcommunity, reflects the interplay between ecological and erances. Because phylogenies summarize the evolutionary evolutionary processes (1, 2). The species composition of a spa- history of the clades within them, phylogeny-based approaches tially defined assemblage depends on the regional species pool, are essential to understanding the origin of variation in species whose composition reflects large-scale biogeographical processes richness across environmental gradients. Here, we analyze, that influence speciation, extinction, and dispersal. A local as- within a phylogenetic context, a comprehensive dataset on the semblage can include only species whose environmental tolerances distributions of seed plants in China. Specifically, we examined allow them to maintain populations under the local abiotic and relationships between indices of phylogenetic structure and biotic conditions of the environment (3, 4). At a broad spatial environment for individual clades, from taxonomic families to scale, environmental filtering is thought to play a strong role in the root of the phylogeny of the Chinese seed plants. We found determining the species composition of an assemblage, whereby that phylogenetic niche conservatism plays an important role in species that cannot survive and reproduce in the local physical the assembly of regional floras in China. environment are excluded (5). The ability of a species to tolerate Author contributions: H.Q. and R.E.R. designed research; H.Q., L.M., D.Z., and R.E.R. per- a particular set of ecological conditions reflects its evolutionary formed research; H.Q., T.D., L.M., and D.Z., compiled data; H.Q., T.D., and Y.J. analyzed history of adaptation. The phylogenetic niche conservatism (PNC) data; and H.Q. and R.E.R. wrote the paper. hypothesis states that species with shared evolutionary history (i.e., Reviewers: Z.T., Peking University; and Y.X., Xishuangbanna Tropical Botanical Garden, species in an evolutionary clade) tend to tolerate similar envi- Chinese Academy of Sciences. ronmental conditions and thus exhibit similar geographic distri- The authors declare no competing interest. butions (6, 7). Accordingly, PNC has important consequences for Published under the PNAS license. the assembly of both local communities and the regional species 1H.Q., T.D., and Y.J. contributed equally to this work. pools from which local communities are assembled (1). The PNC 2To whom correspondence may be addressed. Email: [email protected] or hypothesis [i.e., retention of ecological traits over evolutionary [email protected]. time among related clades or species (8, 9)] predicts that com- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. munities developing under more stressful (e.g., colder, drier, more 1073/pnas.1822153116/-/DCSupplemental. seasonal) conditions should be more strongly structured by envi- First published October 28, 2019. 23192–23201 | PNAS | November 12, 2019 | vol. 116 | no. 46 www.pnas.org/cgi/doi/10.1073/pnas.1822153116 Downloaded by guest on September 25, 2021 For seed plants (Spermatophyta), empirical studies have in- 2) Are the relationships between phylogenetic relatedness and deed shown that phylogenetic relatedness increases, and phylo- climate variables stronger for families that originated in trop- genetic diversity decreases, with decreasing temperature and ical climates than for those that originated in temperate cli- precipitation (e.g., refs. 17 and 18). However, most previous studies mates? Considering that tropical plants are more sensitive to on phylogenetic structure of plant communities have focused ex- cold temperature than are temperate plants, we predict that clusively on angiosperms (flowering plants). All of the families of the relationships between phylogenetic relatedness and cli- gymnosperms—conifers and their relatives—originated long be- mate variables are stronger for ancestrally tropical families fore global climate cooling began in the Eocene. In contrast to (hypothesis H2). angiosperms, which diversified mainly during the late Cretaceous 3) To what extent are the relationships between phylogenetic and Cenozoic, and whose patterns of phylogenetic structure along metrics and environmental variables for individual major environmental gradients are generally consistent with the tropical clades (families, orders, and node-based clades above the niche conservatism hypothesis, gymnosperm diversity and domi- ordinal level) consistent with the tropical niche conservatism nance declined, and many gymnosperm clades went extinct, after hypothesis (i.e., phylogenetic relatedness increases, and phy- the end of the Cretaceous (19). Several living clades of gymno- logenetic diversity decreases, with decreasing temperature sperms are confined to small refugia, suggesting that their cur- and water availability)? Given that predictions from the trop- rent distributions might not be shaped primarily by climate. Thus, ical niche conservatism hypothesis have been confirmed in the relationship between phylogenetic structure and climate for previous studies on angiosperms as a whole
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