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Spatial Patterns and Drivers of Angiosperm Sexual Systems in China Differ Between Woody and Herbaceous Species

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Spatial Patterns and Drivers of Angiosperm Sexual Systems in China Differ Between Woody and Herbaceous Species This is a repository copy of Spatial patterns and drivers of angiosperm sexual systems in China differ between woody and herbaceous species. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/165021/ Version: Published Version Article: Wang, Y., Lyu, T., Luo, A. et al. (5 more authors) (2020) Spatial patterns and drivers of angiosperm sexual systems in China differ between woody and herbaceous species. Frontiers in Plant Science, 11. 1222. https://doi.org/10.3389/fpls.2020.01222 Reuse This article is distributed under the terms of the Creative Commons Attribution (CC BY) licence. This licence allows you to distribute, remix, tweak, and build upon the work, even commercially, as long as you credit the authors for the original work. More information and the full terms of the licence here: https://creativecommons.org/licenses/ Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing [email protected] including the URL of the record and the reason for the withdrawal request. [email protected] https://eprints.whiterose.ac.uk/ ORIGINAL RESEARCH published: 11 August 2020 doi: 10.3389/fpls.2020.01222 Spatial Patterns and Drivers of Angiosperm Sexual Systems in China Differ Between Woody and Herbaceous Species Yunyun Wang 1,2, Tong Lyu 2,3, Ao Luo 2, Yaoqi Li 2, Yunpeng Liu 2, Robert P. Freckleton 4, Shuguang Liu 1 and Zhiheng Wang 2* 1 National Engineering Laboratory for Applied Technology of Forestry & Ecology in Southern China, and College of Life Science and Technology, Central South University of Forest and Technology, Changsha, China, 2 Institute of Ecology and Key Laboratory for Earth Surface Processes of the Ministry of Education, College of Urban and Environmental Sciences, Peking University, Beijing, China, 3 School of Urban Planning and Design, Shenzhen Graduate School, Peking University, Shenzhen, China, 4 Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom Edited by: Hang Sun, Plant sexual systems play an important role in the evolution of angiosperm diversity. Chinese Academy of Sciences, China However, large-scale patterns in the frequencies of sexual systems (i.e. dioecy, monoecy, Reviewed by: Hong Qian, and hermaphroditism) and their drivers for species with different growth forms remain Illinois State Museum, poorly known. Here, using a newly compiled database on the sexual systems and United States Liangsheng Zhang, distributions of 19780 angiosperm species in China, we map the large-scale Zhejiang University, China geographical patterns in frequencies of the sexual systems of woody and herbaceous *Correspondence: species separately. We use these data to test the following two hypotheses: (1) the Zhiheng Wang prevalence of sexual systems differs between woody and herbaceous assemblies [email protected] because woody plants have taller canopies and are found in warm and humid climates; Specialty section: (2) the relative contributions of different drivers (specifically climate, evolutionary age, and This article was submitted to mature plant height) to these patterns differ between woody and herbaceous species. We Functional Plant Ecology, a section of the journal show that geographical patterns in proportions of different sexual systems (especially Frontiers in Plant Science dioecy) differ between woody and herbaceous species. Geographical variations in sexual Received: 10 March 2020 systems of woody species were influenced by climate, evolutionary age and plant height. Accepted: 27 July 2020 In contrast, these have only weakly significant effects on the patterns of sexual systems of Published: 11 August 2020 herbaceous species. We suggest that differences between species with woody and Citation: Wang Y, Lyu T, Luo A, Li Y, Liu Y, herbaceous growth forms in terms of biogeographic patterns of sexual systems, and their Freckleton RP, Liu S and Wang Z drivers, may reflect their differences in physiological and ecological adaptions, as well as (2020) Spatial Patterns and Drivers of Angiosperm Sexual Systems in China the coevolution of sexual system with vegetative traits in response to Differ Between Woody and environmental changes. Herbaceous Species. Front. Plant Sci. 11:1222. Keywords: angiosperms, sexual systems, growth form, climate change, geographical pattern, macro evo-devo, doi: 10.3389/fpls.2020.01222 plant height, China Frontiers in Plant Science | www.frontiersin.org 1 August 2020 | Volume 11 | Article 1222 Wang et al. Patterns of Angiosperm Sexual Systems INTRODUCTION abundance/presence, which may lead to declines of plants populations (Etterson and Mazer, 2016). Moreover, different The sexual systems of plant species play a significant role in the growth forms have contrasting climate preferences. Warm and evolution of angiosperm diversity (Charlesworth and Wright, humid climates are more suitable for woody plants (Wang et al., 2001; Nazareno et al., 2013; Käfer et al., 2014; Sabath et al., 2016; 2011), while herbaceous plants often have broader climate Rosche et al., 2018), variations in reproductive strategies (Bawa, adaptations and hence have widespread distributions (Curtis 1980), and population and community dynamics in response to and Bradley, 2016). Therefore, the influences of climate on climate changes (Queenborough et al., 2009; Wang et al., 2018). sexual system compositions may differ between woody and Understanding the spatial distribution of plant sexual systems herbaceous species. However, the role of climate in driving atlargescalesisvitalforunderstandingthefunctional spatial variations in sexual system compositions of woody and biogeography of reproductive traits. Previous studies have herbaceous species remains poorly understood (Gamble shown that the geographical distributions of angiosperm sexual et al., 2018). systems may ultimately reflect coevolution with vegetative traits Evolutionary history might be expected to influence the that are tied closely to sexual systems (i.e. growth form, Vamosi distribution of sexual systems (Obbard et al., 2006; Barrett, et al., 2003; Moeller et al., 2017; Wang et al., 2020). Nonetheless, 2013; Käfer et al., 2014). Self-pollinated populations likely the determinants of geographical patterns of sexual systems accumulate harmful mutants, which may increase their remain controversial. extinction rate (Etterson and Mazer, 2016). Therefore, self- The evolution of plant sexual systems has been widely pollinated species may be more common in temperate hypothesized to be closely linked to the evolution of plant environments with more short-lived species and younger flora growth forms (e.g. woody vs. herbaceous growth forms, Bawa than in tropical environments. In contrast, dioecy (obligate et al., 1985; Renner and Ricklefs, 1995; Vamosi et al., 2003; outcrossing) can reduce the expression of recessive deleterious Vamosi and Vamosi, 2004; Mitchell and Diggle, 2005; Soza mutations, which tends to reduce their extinction rate (Obbard et al., 2012). Generally, dioecy is significantly more frequent in et al., 2006). Therefore, dioecy may be more frequent in regions woody flowering plant species with long lifespan than in other with older floras. These findings suggest that the composition of growth forms (Renner and Ricklefs, 1995; Sakai et al., 1995; sexual systems within communities is likely associated with the Vamosi et al., 2003; Ward et al., 2005). In contrast, evolutionary ages of species in a region. Additionally, woody hermaphroditism is more common in herbaceous species with and herbaceous species differ significantly in their evolutionary short lifespan (Senarath, 2008; Moeller et al., 2017). This is rates (Laroche et al., 1997; Kay et al., 2006). Woody species likely because obligately outcrossing dioecious species need a have longer reproductive cycles and lifespans, and tend to long lifespan to find mates, reproduce and complete their life accumulate genetic changes more slowly than herbaceous cycle (Morgan et al., 1997; Aarssen, 2000). In contrast, species. Differences in evolutionary rates may lead to hermaphrodites, being able to self-pollinate, are likely to differences in the speed of climate-niche evolution between accumulate more genetic load and suffer from an increased these two growth forms. For example, using more than 5,000 turnover rate (Klekowski and Godfrey, 1989; Chen and Li, plant species, Smith and Beaulieu (2009) found that woody 2008). Moreover, growth form may affect relationships plants adapted to new climates at a rate two to ten times slower between traits and the environment (Fitzjohn et al., 2014). than herbs over the course of their evolution. Therefore, For example, based on more than 88,400 species and six plant exploring the differences between the effects of evolutionary ̌ traits, Sımová ́ et al. (2018) have found significant differences in time on frequencies of sexual systems of woody and herbaceous trait-climate correlations between woody and herbaceous species would improve our understanding of the evolutionary species. However, the biogeographical distributions of sexual mechanisms underlying large-scale patterns in sexual systemsofdifferentgrowthformsacrosslarge-scale system composition. environmental gradients remain poorly understood. Here, using data on sexual systems and spatial distributions of Plant sexual systems and sexual reproduction are sensitive to 19,780 angiosperm species across China, we compare the climate variations (Hedhly et al., 2009; Eckert et al., 2010). geographical
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