The evolution of plant reproductive ecology in China

Scientific interest in plant reproduction has a long and venerable history going back to early European naturalists including Carl Linnaeus, Christian Konrad Sprengel, Joseph Kölreuter, Fritz and Hermann Müller, George Henslow and of course, Charles Darwin. Darwin can be considered the founder of modern plant reproductive biology. His three books (Darwin 1862, 1876, 1877) laid the conceptual foundation for the field, and many of the ideas they contain are still topics of active research (reviewed in Barrett 2010). The turn of the 20th century saw the rediscovery of Mendel’s Laws and breeding experiments on flowering plants played an important role in establishing many key elements of modern genetics. By the 1940s, Fisher had developed the population genetic principles for theoretical analysis of the evolution of plant mating systems (Fisher 1941), and experimental taxonomists were starting to investigate breeding patterns, recognizing that reproductive mode played an important role in governing the patterns of phenotypic variation on which species delimitation was based (Davis and Heywood 1963). Subsequently, the ‘electrophoresis revolution’ (Lewontin 1974), birth of plant population biology (Harper 1977) and development of sex allocation theory (Charnov 1982) each broadened the approaches used in studies of plant reproductive biology. The 1980s saw the coming of age of investigations on the ecology of plant reproduction with the publication of ‘Plant Reproductive Ecology’ (Willson 1983) and ‘Plant Reproductive Ecology: Patterns and Strategies’ (Lovett Doust and Lovett Doust 1988). Today the field is an integral part of evolutionary ecology with articles routinely appearing in the most influential international scientific journals. During much of the 20th century, research in China on plant reproduction focused largely on crop breeding and forestry. Most nonapplied work in plant biology involved the basic subdisciplines (e.g. taxonomy, morphology, physiology and genetics) and the limited number of scientists trained in plant evolutionary ecology meant that this area was largely a backwater that few were prepared to explore. However, the turn of the new millennium in China saw an awakening of interest in the ecology and evolution of plant reproduction. Progress in this area over the past 15 years has been remarkable with a growing number of research groups across China playing an important role in raising the profile of the field, particularly in pollination biology. Useful summaries of Chinese research on pollination are available in Huang and Guo (2000) and Huang (2012). A recent unpublished survey by Ying-Ze Xiong and Shuang-Quan Huang, based on data from Web of Science of global publications in plant reproductive ecology from 2000 to 2014, indicates that articles by Chinese scientists now account for ~6% of the roughly 35 000 that have appeared in this area. Table 1 presents a representative selection of 12 articles published over the past 15 years that in my view have made especially valuable contributions to the diverse areas that comprise modern plant reproductive ecology. selected journal articles on research conducted in China representing diverse topics and approaches in plant reproductive ecology selected journal articles on research conducted in China representing diverse topics and approaches in plant reproductive ecology This special issue of the Journal of Plant Ecology on plant reproductive ecology, edited by my colleagues Shuang-Quan Huang, Wan-Jin Liao and Da-Yong Zhang, is an impressive testimony to the recent accomplishments of Chinese plant ecologists. I was delighted to be asked to write the editorial to this volume and reflect on past accomplishments and future prospects. Over the past 15 years, I have been fortunate to visit China to give lectures, participate in workshops and collaborate with several research groups; these experiences have been among the most rewarding of my academic career. Not only have I benefited considerably from my interactions with students and faculty, but I have also been impressed on each visit by the rapid progress and increasingly diverse approaches being employed to tackle problems in plant reproductive ecology. I begin this editorial with some personal reflections on some of the potential reasons for the explosive growth of plant reproductive ecology in China and then provide a brief summary of some of the exciting work presented in this volume. I conclude with a glimpse into the future and suggest some areas that could be strengthened so that Chinese contributions can move to the forefront of research in this area. What accounts for the impressive growth of plant reproductive ecology in China over the past 15 years? Obviously no single person, event or historical precedent is likely to have been pivotal. Rather, a variety of factors probably played a role, including the value that the Chinese government and its people place on scientific research, the growing concerns about environmental issues and the loss of biodiversity, and the increase in research funding available to plant ecologists. A symposium on plant breeding systems at the International Genetics Congress in Beijing in 1998 can be identified as an early beginning, and gatherings of plant reproductive biologists at Wuhan University in 2001 and 2007, Xishuangbanna Tropical Botanical Garden (XTBG) in 2004, and Beijing Normal University in 2003 and 2006 featuring lectures by invited foreign and Chinese scientists undoubtedly stimulated early interest and collaboration. The meeting in 2006, ‘International Workshop on Plant Reproductive Biology’, organized by Da-Yong Zhang was especially significant because, in addition to formal lectures by Lawrence Harder, Christopher Eckert, John Pannell and myself, it involved a field component at three different locations spanning diverse ecosystems in China (Dongling Mountain, Xiaolongmen National Forest Park, Jade Dragon Field Station near Lijiang and XTBG) where 20–30 Chinese students conducted short field projects on reproductive ecology, some of which have ultimately led to valuable publications (Fig. 1). The great success of the 2006 workshop led to the organization of five subsequent workshops in ‘Plant Reproductive Ecology’ held at Beijing Normal University (2009), Wuhan Botanical Garden (2010), XTBG (2011), Xinjiang Agricultural University, Urumqi (2012) and South China Botanical Garden, Guangzhou (2014) organized by Da-Yong Zhang, Ming-Xun Ren, Jiang-Yun Gao, Dun-Yan Tan and Dian-Xiang Zhang and colleagues, respectively. These workshops have grown in popularity, with ~150 attendees at the 2014 meeting in Guangzhou, and solidified plant reproductive biology as one of the most vibrant areas of research in ecology and evolution in China. : images from the field component of the International Workshop on Plant Reproductive Biology (May 2006) organized by Da-Yong Zhang. (A) Spencer Barrett and students investigating the complex sex expression of Acer pictum subsp. mono at Dongling Mountain (see Shang et al. 2012). (B) Lawrence Harder and Christopher Eckert supervising the data analysis of projects at Dongling Mountain with Shi-Xiao Luo and Shu-Rong Zhou, among others, scrutinizing the results. (C) Bi-Ru Zhu, Yuan-Ye Zhang, Christopher Eckert, Yan-Fei Zeng and Wan-Jin Liao recording the floral characteristics of Rhododendron at the Jade Dragon Field Station near Lijiang. This volume contains 16 articles describing recent research findings in plant reproductive ecology. The topics are diverse and include investigations from a wide range of ecosystems in China including the alpine (6 articles), forests and woodlands (6), weedy habitats (3) and the desert (1) and involving diverse taxa from orchids to oaks as well as several introduced weeds. Most studies involve specific focal species but three take a community-level approach. Nine of the articles involve functional questions related to the adaptive significance of particular traits or patterns of sex allocation and phenology. The popularity of pollination biology in China is evident with 10 articles concerned with some aspect of the pollination process and three investigating pollen limitation of maternal reproductive success. Given the importance of field experiments in plant reproductive ecology it is encouraging that the majority of articles (9) employed some form of experimental manipulation. Below I provide a brief review of the articles in this special issue—highlighting the main findings and also considering unresolved issues. Alpine meadows have always been an attractive setting for research in pollination biology because of the high diversity of animal-pollinated species. The extent of pollen transfer between coflowering species and its influence on plant fitness is an important question in pollination biology (Ashman and Arceo-Gómez 2013; Fang and Huang 2013). Any pollen deposition on stigmas of other species represents a loss of male outcross mating opportunities raising the question of what mechanisms might limit this type of pollen transfer. Huang et al. (2015) investigate the influence of pollinator fidelity and pollen segregation on the bodies of bumblebees as potential mechanisms limiting interspecific pollen transfer in coflowering species of Salvia (Lamiaceae) and Delphinium (Ranuculaceae) in an alpine meadow. They found that the relatively high foraging fidelity and different deposition sites of pollen on the single effective species of Bombus visiting the two species they investigated serve to limit interspecific pollen transfer. This may account for the lack of evidence for any reductions in seed set in open- versus cross-pollinated flowers despite hand crosses showing such effects when interspecific pollen was used. The ecological and evolutionary significance of interspecific pollen transfer in plant communities remains an unresolved question in pollination biology and alpine meadows are an ideal ecological context for these types of investigations. Alpine communities are inevitably composed of species that vary in floral longevity and determining the ecological and evolutionary factors responsible for maintaining variation in flower life spans is an important general question in plant reproductive ecology. Earlier studies established that flower construction and maintenance costs, and the time necessary for fitness accrual through male and female function, play important roles in explaining variation in floral longevity (Schoen and Ashman 1995). In a study of floral longevity in a community of alpine plants, Gao et al. (2015) report that floral sexual investment and dichogamy are also associated with floral longevity. Larger flowers produced more pollen and tended to ‘live’ longer whereas ovule number was not associated with floral longevity. They also found that protandrous species on average exhibited longer floral longevities than adichogamous species, as might be expected because of the temporal requirements for separation of male and female function. Interestingly, in contrast to predictions from sexual selection theory (see Lloyd and Yates 1982) these authors found that the female phase of protandrous species was significantly longer than the male phase, despite the association between the duration of male function, pollen production and floral longevity. Nectar production is an important trait affecting patterns of pollinator foraging, gene dispersal and mating patterns in plant populations. Studies of nectar amounts indicate wide variation within plants and efforts have been directed toward understanding the adaptive significance of this variation (Biernaskie and Cartar 2004). Lu et al. (2015) focus their attention on the correlates of nectar production in protandrous Aconitum gymnandrum (Ranuculaceae), an annual bumblebee-pollinated species of alpine meadows. They confirm the common finding that basal flowers within inflorescences produce more nectar than distal flowers; however, in contrast to most other studies they found no evidence for differences in nectar production between the male and female phases of flowers, or between nectar volume and flower or inflorescence size. In A. gymnandrum attractive traits do not appear to be ‘honest’ signals of the amount of floral rewards, as has been reported in other species and raising the intriguing question as to why this might be. A second article in this special issue also investigates position-dependent influences on floral attributes in A. gymnandrum, but from the perspective of the ecology of sex allocation. Plasticity in sex allocation and gender is a common feature of flowering plants probably because of their immobile habit and occupation of heterogeneous environments (Lloyd and Bawa 1984). One of the predictions of sex allocation theory is that low resource conditions should result in male-biased allocation, but how position-dependent effects on floral investment interact with resource supply has not been investigated within an experimental framework. By manipulating opportunities for resource acquisition through leaf removal in A. gymnandrum, Zhao et al. (2015) demonstrate that allocation to male function increased in more distal flowers within an inflorescence whereas female allocation was unaffected or declined. As the experiment made use of full-sib families, they were also able to demonstrate additive genetic variation for plasticity in floral sex allocation. This is significant as it indicates the potential for selection on sex allocation plasticity if environmental conditions require such a response. The proximate causes and evolutionary consequences of pollen limitation in flowering plants are central problems in reproductive ecology. Over the past decade, considerable progress has been made in our understanding of the prevalence of pollen limitation and the of pollen and limitation of and seed production and Harder et al. have low set and are pollen limited et al. However, relatively few studies have pollinator with of removal and Xiong et al. (2015) conducted an study of this type in in an alpine in China. In most years, no were and the transfer of between plants was However, in three years were and removal and set were set was still pollinator limited based on evidence from The authors suggest that the of may be a adaptive that from pollinator the authors an of in three years and not at other the years of is an intriguing question that remains important question in studies of plant sex allocation is to the common of of investment to and from basal to distal flowers within inflorescences of plants and Huang et al. 2004). this et al. (2015) investigated the roles of pollen and resource limitation in governing patterns of and seed set within inflorescences of and flower removal As this species is a seed set is a of and the influences of in affecting seed production is The authors different patterns of sex allocation than are expected in sexual They found a significant in from basal to distal flowers and suggest that this the of fitness through male function in their species. are few studies of sex allocation in related sexual and species and future investigations on this could provide into the reproductive investment in A wide range of environmental and factors can influence pollen limitation of maternal reproductive success. 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