Why is the beautyberry so colourful? Evolution, biogeography, and diversification of fruit colours in Callicarpa (Lamiaceae)

doi:10.1016/j.pld.2022.10.002

Plant Diversity ›› 2023, Vol. 45 ›› Issue (01): 6-19.DOI: 10.1016/j.pld.2022.10.002

• Research paper • 上一篇下一篇

Why is the beautyberry so colourful? Evolution, biogeography, and diversification of fruit colours in Callicarpa (Lamiaceae)

Xing Liu^a, Hui-Min Cai^a, Wen-Qiao Wang^a, Wei Lin^a, Zhi-Wei Su^b, Zhong-Hui Ma^a

a. Department of Agricultural College, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 530004, Guangxi, PR China;
b. Institute of Marine Drugs, Guangxi University of Chinese Medicine, Nanning 530004, Guangxi, PR China

收稿日期:2022-04-27 修回日期:2022-10-04 发布日期:2023-02-23
通讯作者: Zhong-Hui Ma,E-mail:mazhonghui@gxu.edu.cn
基金资助:
This research was funded by National Natural Science Foundation of China under Grant [31760045 and 31970220] and Natural Science Foundation of Guangxi Province under Grant [2018GXNSFAA281132].

Why is the beautyberry so colourful? Evolution, biogeography, and diversification of fruit colours in Callicarpa (Lamiaceae)

Xing Liu^a, Hui-Min Cai^a, Wen-Qiao Wang^a, Wei Lin^a, Zhi-Wei Su^b, Zhong-Hui Ma^a

a. Department of Agricultural College, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 530004, Guangxi, PR China;
b. Institute of Marine Drugs, Guangxi University of Chinese Medicine, Nanning 530004, Guangxi, PR China

Received:2022-04-27 Revised:2022-10-04 Published:2023-02-23
Contact: Zhong-Hui Ma,E-mail:mazhonghui@gxu.edu.cn
Supported by:
This research was funded by National Natural Science Foundation of China under Grant [31760045 and 31970220] and Natural Science Foundation of Guangxi Province under Grant [2018GXNSFAA281132].

摘要/Abstract

摘要： Fruit colour is essential to seed dispersal, speciation, and biological diversity in global ecosystems. The relationship between fruit-colour variation and species diversification has long been of interest in evolutionary biology, but remains poorly understood at the genus level. Here, we used Callicarpa, a typical representative of pantropical angiosperm, to analyse whether fruit colours are correlated with biogeographic distribution, dispersal events, and diversification rate. We estimated a time-calibrated phylogeny for Callicarpa and reconstructed ancestral fruit colour. Utilizing phylogenetic methods, we estimated the major dispersal events across the phylogenetic tree and the most likely fruit colours related to each dispersal event, and tested whether the dispersal frequencies and distances of the four fruit colours between major biogeographical areas were equal. We then tested whether fruit colours are correlated with latitude, elevation, and diversification rate. Biogeographical reconstructions showed that Callicarpa originated in the East Asia and Southeast Asia during the Eocene (~35.53 Ma) and diverse species diverged mainly in the Miocene and lasted into the Pleistocene. Large-scale dispersal events were significantly associated with violet-fruited lineages. Furthermore, different fruit colours were markedly correlated with different latitudes and elevations (e.g., violet fruits were correlated with higher latitudes and elevations; red fruits and black fruits with lower latitudes; white fruits with higher elevations). Notably, violet fruits were statistically associated with highest diversification rates, driving fruit colour variation among different regions globally. Our results contribute to further understanding why fruit colour is so variable at the genus level of angiosperms in different areas around the world.

关键词: Callicarpa, Fruit colour, Phylogeny, Biogeography, Dispersal, Diversification

Abstract: Fruit colour is essential to seed dispersal, speciation, and biological diversity in global ecosystems. The relationship between fruit-colour variation and species diversification has long been of interest in evolutionary biology, but remains poorly understood at the genus level. Here, we used Callicarpa, a typical representative of pantropical angiosperm, to analyse whether fruit colours are correlated with biogeographic distribution, dispersal events, and diversification rate. We estimated a time-calibrated phylogeny for Callicarpa and reconstructed ancestral fruit colour. Utilizing phylogenetic methods, we estimated the major dispersal events across the phylogenetic tree and the most likely fruit colours related to each dispersal event, and tested whether the dispersal frequencies and distances of the four fruit colours between major biogeographical areas were equal. We then tested whether fruit colours are correlated with latitude, elevation, and diversification rate. Biogeographical reconstructions showed that Callicarpa originated in the East Asia and Southeast Asia during the Eocene (~35.53 Ma) and diverse species diverged mainly in the Miocene and lasted into the Pleistocene. Large-scale dispersal events were significantly associated with violet-fruited lineages. Furthermore, different fruit colours were markedly correlated with different latitudes and elevations (e.g., violet fruits were correlated with higher latitudes and elevations; red fruits and black fruits with lower latitudes; white fruits with higher elevations). Notably, violet fruits were statistically associated with highest diversification rates, driving fruit colour variation among different regions globally. Our results contribute to further understanding why fruit colour is so variable at the genus level of angiosperms in different areas around the world.

Key words: Callicarpa, Fruit colour, Phylogeny, Biogeography, Dispersal, Diversification

Xing Liu, Hui-Min Cai, Wen-Qiao Wang, Wei Lin, Zhi-Wei Su, Zhong-Hui Ma. Why is the beautyberry so colourful? Evolution, biogeography, and diversification of fruit colours in Callicarpa (Lamiaceae)[J]. Plant Diversity, 2023, 45(01): 6-19.

参考文献

[1] Areces-Berazain, Fabiola., James, D.Ackerman., 2017. Diversification and fruit evolution in eumalvoids (Malvaceae). Bot. J. Linn. Soc. 184, 401-417
[2] Beaulieu, J.M., Donoghue, M.J., 2013. Fruit evolution and diversification in campanulid angiosperms. Evolution 67, 3132-3144
[3] Bogert, C.M., 1949. Thermoregulation in reptiles, a factor in evolution. Evolution 3, 195-211
[4] Bollback, J.P., 2006. SIMMAP:stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7, 88
[5] Bouckaert, R., Heled, J., Kuhnert, D., et al. 2014. BEAST 2:a software platform for Bayesian Evolutionary Analysis. PLoS Comput. Biol. 10, e1003537
[6] Bramley, G.L.C., 2009. The genus Callicarpa (Lamiaceae) on Borneo. Bot. J. Linn. Soc. 159, 416-455
[7] Bramley, G.L.C., 2011. Distribution patterns in Malesian Callicarpa (Lamiaceae). Garden Bull. Singap. 63, 287-298
[8] Bremer, K., 1992. Ancestral areas:a cladistic reinterpretation of the center of origin concept. Syst. Biol. 41, 436-445
[9] Burns, K.C., 2015. The color of plant reproduction:macroecological trade-offs between biotic signaling and abiotic tolerance. Front. Ecol. Evol. 3, 118
[10] Campanella, J.J., Smalley, J.V., Dempsey, M.E., 2014. A phylogenetic examination of the primary anthocyanin production pathway of the Plantae. Bot. Stud. 55, 1-10
[11] Cantley, J.T., Markey A.S., Swenson, N.G., et al., 2016. Biogeography and evolutionary diversification in one of the most widely distributed and species rich genera of the Pacific. Aob Plants 8, 16
[12] Cantrell, C.L., Klun, J.A., Bryson, C.T., et al., 2005. Isolation and identification of mosquito bite deterrent terpenoids from leaves of American (Callicarpa americana) and Japanese (Callicarpa japonica) beautyberry. J. Agr. Food Chem. 53, 5948-5953
[13] Cavanaugh, J.E., 1997. Unifying the derivations for the Akaike and corrected Akaike information criteria. Stat. Probabil. Lett. 33, 201-208
[14] Cazetta, E., Schaefer, H.M., Galetti, M., 2008. Does attraction to frugivores or defense against pathogens shape fruit pulp composition? Oecologia 155, 277-286
[15] Chalker-Scott, L., 1999. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 70, 1-9
[16] Chen, S.L., Michael, G.G., 1994. Flora of China, in:Wu Z. Y., & P. H. Raven (eds), Verbenaceae. Science Press & St. Louis:Missouri Botanical Garden Press, Beijing, pp. 25-79
[17] Chen, S.C., Cornwell, W.K., Zhang, H.X., et al., 2017. Plants show more flesh in the tropics:variation in fruit type along latitudinal and climatic gradients. Ecography 40, 531-538
[18] Chung, I.M., Ali, M., Upadhayay, K., et al., 2005. Isolation and cytotoxic activity of acyclic triterpene callicarpenol from Callicarpa macrophylla. Asian J. Org. Chem. 17, 1907-1914
[19] Cuthill, I.C., 2015. Flower colour:Gloger's rule isn't just for the birds. Nat. Plants 1, 1-2
[20] Dodd, M.E., J, Silvertown., Chase, M.W., 1999. Phylogenetic analysis of trait evolution and species diversity variation among angiosperm families. Evolution 53, 732-744
[21] Donoghue, M.J., Smith, S.A., 2004. Patterns in the assembly of temperate forests around the Northern Hemisphere. Philos. T. R. Soc. B. 359, 1633-1644
[22] Doyle, J.J., Doyle, J.D., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15
[23] Drew, B.T., Sytsma, K.J., 2012. Phylogenetics, biogeography, and staminal evolution in the tribe mentheae (Lamiaceae). Am. J. Bot. 99, 933-953
[24] Drummond, A.J., Suchard, M.A., Xie, D., et al., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973
[25] Ebersbach, J., Schnitzler, J., Favre, A., et al., 2017. Evolutionary radiations in the species-rich mountain genus Saxifraga L. BMC Evol. Biol. 17, 119
[26] Eriksson, O., B, Bremer., 1991. Fruit characteristics, life forms, and species richness in the plant family Rubiaceae. Am. Nat. 138, 751-761
[27] Fricke, E.C., Svenning, J.C., 2020. Accelerating homogenization of the global plant-frugivore meta-network. Nature 585, 74-78
[28] Gao, J., Liao, P.C., Huang, B.H., et al., 2020. Historical biogeography of Acer L. (Sapindaceae):genetic evidence for Out-of-Asia hypothesis with multiple dispersals to North America and Europe. Sci. Rep. 10, 1-10
[29] Glor, R.E., 2010. Phylogenetic insights on adaptive radiation. Annu. Rev. Ecol. Evol. Syst. 41, 251-270
[30] Gould, K.S., 2004. Nature's Swiss army knife:the diverse protective roles of anthocyanins in leaves. J. Biomed. Biotechnol. 2004, 314-320
[31] Harris, A.J., Xiang, Q.Y., 2009. Estimating ancestral distributions of lineages with uncertain sister groups:a statistical approach to Dispersal-Vicariance Analysis and a case using Aesculus L. (Sapindaceae) including fossils. J. Syst. Evol. 47, 349-368
[32] Harrison, T.M., Copeland, P., Kidd, W.S.F., et al., 1992. Raising tibet. Science 255, 1663-1670
[33] Herrera, C.M., 1989. Seed dispersal by animals:a role in angiosperm diversification? Am. Nat. 133, 309-322
[34] Hill, A.P., Jimenez, M.F.T., Chazot, N., et al., 2021. Fruit colour and range size interact to influence diversification. bioRxiv
[35] Holt, B.G., Lessard, J.P., Borregaard, M.K., et al., 2013. Response to comment on "An update of Wallace's zoogeographic regions of the world". Science 341, 343-343
[36] Hughes, C., Eastwood, R., 2006. Island radiation on a continental scale:exceptional rates of plant diversification after uplift of the Andes. Proc. Natl. Acad. Sci. U.S.A. 103, 10334-10339
[37] Hutter, C.R., Lambert, S.M., Wiens, J.J., 2017. Rapid diversification and time explain amphibian richness at different scales in the Tropical Andes, Earth's most biodiverse hotspot. Am. Nat. 190, 828-843
[38] Jaa, A.A., 2004. MrModeltest v. 2 (program distributed by the author)
[39] Jafari, M., Ansari-Pour, N., 2019. Why, when and how to adjust your P values? Cell J. 20, 604
[40] Janson, C.H., 1983. Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219, 187-189
[41] Jansson, R., Davies, T.J., 2008. Global variation in diversification rates of flowering plants:energy vs. climate change. Ecol. Lett. 11, 173-183
[42] Jetz, W., Thomas, G.H., Joy, J.B., et al., 2012. The global diversity of birds in space and time. Nature 491, 444-448
[43] Jordano, P., Garcia, C., Godoy, J.A., et al., 2007. Differential contribution of frugivores to complex seed dispersal patterns. Proc. Natl. Acad. Sci. U.S.A. 104, 3278-3282
[44] Kar, R., 1996. On the Indian origin of Ocimum (Lamiaceae):A palynological approach. Palaeobotanist 43, 43-50
[45] Kemp, D.J., Herberstein, M.E., Fleishman, L.J., et al., 2015. An integrative framework for the appraisal of coloration in nature. Am. Nat. 185:705-724
[46] Klaus, K.V., Matzke, N.J., 2020. Statistical comparison of trait-dependent biogeographical models indicates that podocarpaceae dispersal is influenced by both seed cone traits and geographical distance. Syst. Biol. 69, 61-75
[47] Kong, H., Condamine, F.L., Yang, L., et al., 2022. Phylogenomic and macro-evolutionary evidence for an explosive radiation of a plant genus in the Miocene. Syst. Biol. 71, 589-609
[48] Kozak, K.H., Wiens, J.J., 2016. Testing the relationships between diversification, species richness, and trait evolution. Syst. Biol. 65, 975-988
[49] Lagomarsino, L.P., Condamine, F.L., Antonelli, A., et al., 2016. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytol. 210, 1430-1442
[50] Landis, M.J., Matzke, N.J., Moore, B.R., et al., 2013. Bayesian analysis of biogeography when the number of areas is large. Syst. Biol. 62, 789-804
[51] Landis, M.J., Freyman, W.A., Baldwin, B.G., 2018. Retracing the Hawaiian silversword radiation despite phylogenetic, biogeographic, and paleogeographic uncertainty. Evolution 72, 2343-2359
[52] Latti, A.K., Riihinen, K.R., Kainulainen, P.S., 2008. Analysis of anthocyanin variation in wild populations of bilberry (Vaccinium myrtillus L.) in Finland. J. Agr. Food Chem. 56, 190-196
[53] Li, B., Cantino, P.D., Olmstead, R.G., et al., 2016. A large-scale chloroplast phylogeny of the Lamiaceae sheds new light on its subfamilial classification. Sci. Rep. 6, 1-18
[54] Lu, L., Fritsch, P.W., Matzke, N.J., et al., 2019. Why is fruit colour so variable? Phylogenetic analyses reveal relationships between fruit-colour evolution, biogeography and diversification. Global Ecol. Biogeogr. 28, 891-903
[55] MacKinnon, J.R., MacKinnon, J., Phillipps, K., et al., 2000. A field guide to the birds of China. Oxford University Press
[56] Mahler, D.L., Revell, L.J., Glor, R.E., et al., 2010. Ecological opportunity and the rate of morphological evolution in the diversification of Greater Antillean anoles. Evolution 64, 2731-2745
[57] Martinez-Millan, M., 2010. Fossil record and age of the Asteridae. Bot. Rev. 76, 83-135
[58] McGuire, J.A., Witt, C.C., Remsen, J.V., et al. 2014. Molecular phylogenetics and the diversification of hummingbirds. Curr. Biol. 24, 1038-1038
[59] Miller, M.A., Pfeiffer, W., Schwartz, T., 2010. The CIPRES science gateway:a community resource for phylogenetic analyses. Proceedings of the 2011 TeraGrid Conference:extreme digital discovery 2011, 1-8
[60] Moen, D., Morlon, H., 2014. Why does diversification slow down? Trends Ecol. Evol. 29, 190-197
[61] Moore, B.R., Hohna, S., May, M.R., et al., 2016. Critically evaluating the theory and performance of Bayesian analysis of macroevolutionary mixtures. Proc. Natl. Acad. Sci. U.S.A. 113, 9569-9574
[62] Nakagawa, S., 2004. A farewell to Bonferroni:the problems of low statistical power and publication bias. Behav. Ecol. 15, 1044-1045
[63] Nakanishi, H., 1996. Fruit color and fruit size of bird-disseminated plants in Japan. J. Veg. Sci. 123, 207-218
[64] Nishi, H., Tsuyuzaki, S., 2004. Seed dispersal and seedling establishment of Rhus trichocarpa promoted by a crow (Corvus macrorhynchos) on a volcano in Japan. Ecography 27, 311-322
[65] Nylander, J.A., Olsson, U., Alstrom, P., et al., 2008. Accounting for phylogenetic uncertainty in biogeography:a Bayesian approach to dispersal-vicariance analysis of the thrushes (Aves:Turdus). Syst. Biol. 57, 257-268
[66] Paradis, E., Claude, J., Strimmer, K., 2004. APE:Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20, 289-290
[67] Pyron, R.A., Wiens, J.J., 2013. Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. P. Roy. Soc. B-Biol. Sci. 280, 20131622
[68] Qian, C.J., Shi, Y., Liu, Y., et al., 2018. Phylogenetics and dispersal patterns of Brassicaceae around the Qinghai-Tibet Plateau. J. Syst. Evol. 56, 202-217
[69] Rabosky, D.L., Donnellan, S.C., Grundler, M., et al., 2014a. Analysis and visualization of complex macroevolutionary dynamics:an example from Australian scincid lizards. Syst. Biol. 63, 610-627
[70] Rabosky, D.L., Grundler, M., Anderson, C., et al. 2014b. BAMMtools:an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 5, 701-707
[71] Rambaut, A., Drummond, A.J., Xie, D., 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901
[72] Reguera, S., Zamora-Camacho, F.J., Moreno-Rueda, G., 2014. The lizard Psammodromus algirus (Squamata:Lacertidae) is darker at high altitudes. Biol. J. Linn. Soc. 112, 132-141
[73] Revell, L.J., 2012. Phytools:an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223
[74] Rolland, J., Condamine, F.L., Jiguet, F., et al., 2014. Faster speciation and reduced extinction in the tropics contribute to the mammalian latitudinal diversity gradient. PLoS Biology 12, e1001775
[75] Schaefer, H.M., McGraw, K., Catoni, C., 2008. Birds use fruit colour as honest signal of dietary antioxidant rewards. Funct. Ecol. 22, 303-310
[76] Schaefer, H.M., Valido, A., Jordano, P., 2014. Birds see the true colours of fruits to live off the fat of the land. P. Roy. Soc. B-Biol. Sci. 281, 20132516
[77] Shanahan, M., So, S., Compton, S.G., et al., 2001. Fig-eating by vertebrate frugivores:a global review. Biol. Rev. 76, 529-572
[78] Shaw, J., Lickey, E.B., Beck, J.T., et al., 2005. The tortoise and the hare II:relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am. J. Bot. 92, 142-166
[79] Shaw, J., Lickey, E.B., Schilling, E.E., et al., 2007. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms:the tortoise and the hare III. Am. J. Bot. 94, 275-288
[80] Sinnott-Armstrong, M.A., Downie, A.E., Federman, S., et al., 2018. Global geographic patterns in the colours and sizes of animal-dispersed fruits. Global Ecol. Biogeogr. 27, 1339-1351
[81] Sinnott-Armstrong, M.A., Lee, C., Clement, W.L., et al., 2020. Fruit syndromes in Viburnum:correlated evolution of color, nutritional content, and morphology in bird-dispersed fleshy fruits. BMC Evol. Biol. 20, 1-19
[82] Sinnott-Armstrong, M.A., Donoghue, M.J., Jetz, W.J., 2021. Dispersers and environment drive global variation in fruit colour syndromes. Ecol. Lett. 24, 1387-1399
[83] Smith, J.F., 2001. High species diversity in fleshy-fruited tropical understory plants. Am. Nat. 157, 646-653
[84] Smith, S.B., DeSando, S.A., Pagano, T., 2013. The value of native and invasive fruit-bearing shrubs for migrating songbirds. Northeast. Nat. 20, 171-184
[85] Sotomayor, D.A., 2014. Biotic evolution and environmental change in Southeast Asia. Can. Geogr-Geogr. Can. 58, E58-E58
[86] Spriggs, E.L., Clement, W.L., Sweeney, P.W., et al., 2015. Temperate radiations and dying embers of a tropical past:the diversification of Viburnum. New Phytol. 207, 340-354
[87] Steyn, W.J., Wand, S.J.E., Holcroft, D.M., et al., 2002. Anthocyanins in vegetative tissues:a proposed unified function in photoprotection. New Phytol. 155, 349-361
[88] Steyn, W.J., Wand, S.J.E., Jacobs, G., et al., 2009. Evidence for a photoprotective function of low-temperature-induced anthocyanin accumulation in apple and pear peel. Physiol. Plantarum 136, 461-472
[89] Sullivan, D., 2009. Google Earth Pro. Econtent 32, 16-18
[90] Tiffney, B.H., Mazer, S.J., 1995. Angiosperm growth habit, dispersal and diversification reconsidered. Evol. Ecol. 9, 93-117
[91] Tu, Y.H., Sun, L.N., Guo, M.L., et al., 2013. The medicinal uses of Callicarpa L. in traditional Chinese medicine:An ethnopharmacological, phytochemical and pharmacological review. J. Ethnopharmacol. 146, 465-481
[92] Valenta, K., Nevo, O., 2020. The dispersal syndrome hypothesis:how animals shaped fruit traits, and how they did not. Funct. Ecol. 34, 1158-1169
[93] Van Dam, M.H., Matzke, N.J., 2016. Evaluating the influence of connectivity and distance on biogeographical patterns in the south-western deserts of North America. J. Biogeogr. 43, 1514-1532
[94] Van Iterson, M., Boer, J.M., Menezes, R.X., 2010. Filtering, FDR and power. BMC bioinformatics 11, 1-11
[95] Vittoz, P., Dussex, N., Wassef, J., et al., 2009. Diaspore traits discriminate good from weak colonisers on high-elevation summits. Basic Appl. Ecol. 10, 508-515
[96] Wheelwright, N.T., 1988. Fruit-eating birds and bird-dispersed plants in the tropics and temperate zone. Trends Ecol. Evol. 3, 270-274
[97] Willson, M.F., Irvine, A.K., Walsh, N.G., 1989. Vertebrate dispersal syndromes in some Australian and New Zealand plant-communities, with geographic comparisons. Biotropica 21, 133-147
[98] Willson, M.F., Graff, D.A., Whelan, C.J., 1990a. Color preferences of frugivorous birds in relation to the colors of fleshy fruits. Condor 92, 545-555
[99] Willson, M.F., Rice, B.L., Westoby, M., 1990b. Seed dispersal spectra:a comparison of temperate plant communities. J. Veg. Sci. 1, 547-562
[100] Willson, M.F., Sabag, C., Figueroa, J., et al., 1996. Seed dispersal by lizards in Chilean rainforest. Rev. Chil. Hist. Nat. 69, 339-342
[101] Wolfe J.A., 1978. A paleobotanical interpretation of Tertiary climates in the Northern Hemisphere:Data from fossil plants make it possible to reconstruct Tertiary climatic changes, which may be correlated with changes in the inclination of the earth's rotational axis. Am. Sci. 66, 694-703
[102] Wolfe J.A., Schorn H.E., Forest C.E., et al., 1997. Paleobotanical evidence for high altitudes in Nevada during the Miocene. Science 276, 1672-1675
[103] Xing, Y.W., Ree, R.H., 2017. Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc. Natl. Acad. Sci. U.S.A. 114, E3444-E3451
[104] Ye, X.Y., Ma, P.F., Yang, G.Q., et al., 2019. Rapid diversification of alpine bamboos associated with the uplift of the Hengduan Mountains. J. Biogeogr. 46, 2678-2689
[105] Yoder, J.B., Clancey E., Des Roches, S., et al., 2010. Ecological opportunity and the origin of adaptive radiations. J. Evol. Biol. 23, 1581-1596
[106] Young, L.M., Kelly, D., Nelson, X.J., 2012. Alpine flora may depend on declining frugivorous parrot for seed dispersal. Biol. Conserv. 147, 133-142
[107] Yu, Y., Harris, A.J., Blair, C., et al., 2015. RASP (Reconstruct Ancestral State in Phylogenies):a tool for historical biogeography. Mol. Phylogenet. Evol. 87, 46-49
[108] Zhang, Y.B., Li, X., Zhang, F., et al., 2012. A preliminary study of copy number variation in Tibetans. PLoS One 7, e41768
[109] Zoratti, L., Karppinen, K., Escobar, A.L., et al., 2014. Light-controlled flavonoid biosynthesis in fruits. Front. Plant Sci. 5, 534

Why is the beautyberry so colourful? Evolution, biogeography, and diversification of fruit colours in Callicarpa (Lamiaceae)

Why is the beautyberry so colourful? Evolution, biogeography, and diversification of fruit colours in Callicarpa (Lamiaceae)

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 15

编辑推荐

Metrics

本文评价

[1]	Xin-Mao Zhou, Li-Bing Zhang. Phylogeny, character evolution, and classification of Selaginellaceae(lycophytes)[J]. Plant Diversity, 2023, 45(06): 630-684.
[2]	Zhe Chen, Zhuo Zhou, Ze-Min Guo, Truong Van Do, Hang Sun, Yang Niu. Historical development of karst evergreen broadleaved forests in East Asia has shaped the evolution of a hemiparasitic genus Brandisia (Orobanchaceae)[J]. Plant Diversity, 2023, 45(05): 501-512.
[3]	Hai-Su Hu, Jiu-Yang Mao, Xue Wang, Yu-Ze Liang, Bei Jiang, De-Quan Zhang. Plastid phylogenomics and species discrimination in the “Chinese” clade of Roscoea (Zingiberaceae)[J]. Plant Diversity, 2023, 45(05): 523-534.
[4]	Korina Ocampo-Zuleta, Ángela Parrado-Rosselli. Functional diversity in an Andean subpáramo affected by wildfire in Colombia[J]. Plant Diversity, 2023, 45(04): 385-396.
[5]	Yu-Feng Gu, Jiang-Ping Shu, Yi-Jun Lu, Hui Shen, Wen Shao, Yan Zhou, Qi-Meng Sun, Jian-Bing Chen, Bao-Dong Liu, Yue-Hong Yan. Insights into cryptic speciation of quillworts in China[J]. Plant Diversity, 2023, 45(03): 284-301.
[6]	Yi Jin, Hong Qian. U.PhyloMaker:An R package that can generate large phylogenetic trees for plants and animals[J]. Plant Diversity, 2023, 45(03): 347-352.
[7]	Li-Guo Zhang, Xiao-Qian Li, Wei-Tao Jin, Yu-Juan Liu, Yao Zhao, Jun Rong, Xiao-Guo Xiang. Asymmetric migration dynamics of the tropical Asian and Australasian floras[J]. Plant Diversity, 2023, 45(01): 20-26.
[8]	Han-Yang Lin, Miao Sun, Ya-Jun Hao, Daijiang Li, Matthew A. Gitzendanner, Cheng-Xin Fu, Douglas E. Soltis, Pamela S. Soltis, Yun-Peng Zhao. Phylogenetic diversity of eastern Asia-eastern North America disjunct plants is mainly associated with divergence time[J]. Plant Diversity, 2023, 45(01): 27-35.
[9]	Mei-Zhen Wang, Xiao-Kai Fan, Yong-Hua Zhang, Jing Wu, Li-Mi Mao, Sheng-Lu Zhang, Min-Qi Cai, Ming-Hong Li, Zhang-Shi-Chang Zhu, Ming-Shui Zhao, Lu-Xian Liu, Kenneth M. Cameron, Pan Li. Phylogenomics and integrative taxonomy reveal two new species of Amana (Liliaceae)[J]. Plant Diversity, 2023, 45(01): 54-68.
[10]	Sanchita Kumar, Taposhi Hazra, Robert A. Spicer, Manoshi Hazra, Teresa E. V. Spicer, Subir Bera, Mahasin Ali Khan. Coryphoid palms from the K-Pg boundary of central India and their biogeographical implications: Evidence from megafossil remains[J]. Plant Diversity, 2023, 45(01): 80-97.
[11]	Hong-Hu Meng, Can-Yu Zhang, Shook Ling Low, Lang Li, Jian-Yong Shen, Nurainas, Yu Zhang, Pei-Han Huang, Shi-Shun Zhou, Yun-Hong Tan, Jie Li. Two new species from Sulawesi and Borneo facilitate phylogeny and taxonomic revision of Engelhardia (Juglandaceae)[J]. Plant Diversity, 2022, 44(06): 552-564.
[12]	Yi Jin, Hong Qian. V.PhyloMaker2：An updated and enlarged R package that can generate very large phylogenies for vascular plants[J]. Plant Diversity, 2022, 44(04): 335-339.
[13]	Jun-Hao Yu, Rui Zhang, Qiao-Ling Liu, Fa-Guo Wang, Xun-Lin Yu, Xi-Ling Dai, Yong-Bo Liu, Yue-Hong Yan. Ceratopteris chunii and Ceratopteris chingii (Pteridaceae), two new diploid species from China, based on morphological, cytological, and molecular data[J]. Plant Diversity, 2022, 44(03): 300-307.
[14]	Lei Huang, Fang-Dong Geng, Jing-Jing Fan, Wei Zhai, Cheng Xue, Xiao-Hui Zhang, Yi Ren, Ju-Qing Kang. Evidence for two types of Aquilegia ecalcarata and its implications for adaptation to new environments[J]. Plant Diversity, 2022, 44(02): 153-162.
[15]	Changkyun Kim, Dong-Kap Kim, Hang Sun, Joo-Hwan Kim. Phylogenetic relationship, biogeography, and conservation genetics of endangered Fraxinus chiisanensis (Oleaceae), endemic to South Korea[J]. Plant Diversity, 2022, 44(02): 170-180.