The ecology, evolution, and genetics of plant reproductive systems

Reproduction forms the link between generations and is fundamental to the evolution and ecology of organisms. During the past four decades we have witnessed an explosion of research on plant reproductive systems that has enriched the study of ecology and evolution. An important igniting spark was the introduction of theoretical modelling into the field (Lloyd, 1975, 1979; B. Charlesworth & D. Charlesworth, 1978; D. Charlesworth & B. Charlesworth, 1979). This development marked a move away from viewing the evolution of reproductive systems, through the lens of group selection, to one that instead considers selection at the gene and individual levels, especially the selection of modifiers of the mating system. This shift in perspective led to innovative ways of framing questions about how ecological and genetic aspects of plant populations influence the evolution of reproductive systems and paved the way for a large number of experimental studies in the laboratory and field, merging pollination biology, quantitative genetics, comparative biology, phylogenetics, population genetics and, most recently, genomics. Combining these approaches allowed researchers to address specific questions about the interrelationships between plant reproductive systems and pollination, the consequences of mating patterns for the genetic composition of populations and evolution of traits, the evolutionary history of reproductive systems and their influence on speciation and extinction dynamics. This impressive synthesis has in large part been led by our colleague Professor Spencer Barrett and his many students, postdoctoral fellows and collaborators. Fittingly, the idea behind this Special Issue arose from a symposium that celebrated Spencer's retirement from the University of Toronto (Canada) after 40 years, and from the recognition that as the field continues to grow it is an opportune moment to take stock of recent developments and new directions. The symposium was held at the University of Toronto on 10–11 August 2018 and was entitled 'Evolution of plant reproductive systems: from muddy boots to genomics'; a title which signifies the multifaceted nature of research in this field, which integrates ecology, evolution and genetics of plant reproduction (Fig. 1). It is our hope that the papers published here by speakers at the symposium and others who submitted their work capture some of the richness of the field and will aid in stimulating new research avenues. Spencer Barrett's research on plant reproductive systems has been an inspiration to many students, collaborators and colleagues. While the study of plant reproductive systems clearly benefits from an integrated approach, it is rare for a single research program to span the breadth of the field. Many of us focus on one aspect, such as microevolution, while treating the ecology, macroevolution, or genomics as a black box. Spencer's research program has been unique in seamlessly merging these disciplines to answer diverse questions on the ecology and evolution of plant reproductive systems. His earliest work as a PhD student focused on the maintenance and breakdown of heterostyly, a topic that he has worked on throughout his career (Barrett, 1990; Barrett, 2019 in this issue, pp. 1051–1067) and he and his students have elegantly demonstrated the combined role of pollinator shifts, population demography, and the genetics of heterostyly, in governing the evolutionary trajectory of this classic polymorphism (Barrett, 1979; Barrett & Glover, 1985; Shore & Barrett, 1985). Spencer's contributions extend across the full breadth of the ecology and evolution of plant reproductive systems (Barrett, 2002). As a young professor at the University of Toronto, his laboratory characterized the ecology and evolution of plant mating and sexual systems in many plant species in the woodlands and wetlands of Canada (Thomson & Barrett, 1981; Barrett & Thomson, 1982; Eckert & Barrett, 1994; Larson & Barrett, 1999). Even as a student, Spencer's interests and approaches were broader than any one scientific problem or approach. For example, while a graduate student at UC Berkeley in the 1970s, he developed an early fascination with the now burgeoning field of invasion biology, and here again he combined ecological, evolutionary and genetic approaches to understand how species succeed in novel environments. He used this approach to address such problems as how plants can evolve to mimic crop plants (Barrett, 1983), how plant reproductive strategies contribute to their invasiveness (Barrett, 1992a,b; Barrett et al., 2008; Colautti et al., 2010), and how species adapt to environmental gradients in their new ranges (Colautti & Barrett, 2011, 2013). Similarly, his research on the evolution of combined versus separate sexes (Barrett, 1992a,b; Dorken & Barrett, 2004; Case et al., 2008; Yakimowski & Barrett, 2014), and the evolution of sex ratios (Stehlik & Barrett, 2005; Pickup & Barrett, 2011) incorporate ecological, theoretical and genetic dimensions to the problem at hand, in addition to consideration of both micro- and macroevolutionary scales. While a major focus of his career has been on microevolutionary changes within species to conduct powerful tests of evolutionary transitions, Spencer has been equally comfortable with macroevolutionary perspectives on these problems (Graham et al., 1998; Friedman & Barrett, 2008), recognizing early on the power of the comparative method for studies on plant reproduction (Barrett et al., 1996). His research has also contributed new insights into the consequences of interference between the male and female sex roles for the evolution of floral and inflorescence architecture (Harder & Barrett, 1995; Worley & Barrett, 2000; Jesson & Barrett, 2002). More recently he has embraced genomic technology to address the joint roles of genetic drift, gene flow and natural selection in shaping the evolution of plant reproductive systems (Ness et al., 2010, 2011; Barrett et al., 2014; Hough et al., 2014; Arunkumar et al., 2015; Crowson et al., 2017). In such a brief overview it is difficult to do justice to Spencer's many contributions to plant evolutionary biology, though some final points about the approach that Spencer has taken to science deserve special mention as they relate to his style of collaboration and mentorship. Spencer has never allowed political borders to constrain his research, having published papers based on research in many countries, including with numerous collaborators in China, Australia, South Africa, and many countries in Europe and South America. The international flavour is clearly visible in this Special Issue. As a supervisor, Spencer has helped to train many of the next generation of scientists. For example, he mentored over 40 graduate students and postdoctoral fellows, many of whom have gone on to independent research. Spencer's mentorship does not stop at his own lab, as he has taught and continues to teach many international field courses and workshops, and generously has helped the careers of many young scientists who were not directly in his lab. Few in recent memory have had an impact as large and left a legacy as strong in plant evolutionary biology. This Special Issue is meant to highlight this impact, covering the breadth of Spencer's approaches to the study of the ecology, evolution and genetics of plant reproductive systems as outlined below. The ecological context in which plant reproductive systems evolve has long been the focus of research in the plant sciences. For example, Puixeu et al. (2019, in this issue pp 1108–1120) investigate the role of environmental heterogeneity in determining the degree of sexual dimorphism in a dioecious system, highlighting strong correlates of abiotic climate conditions with patterns of sexual dimorphism. Several papers in this Special Issue address questions about the interaction of flowers with their environment, especially their pollen vectors. Vallejo-Marín (2019, in this issue pp. 1068–1074) and Timerman & Barrett (2019, in this issue pp. 1121–1132) explore pollination within the context of the interaction with bees and wind, respectively. These papers demonstrate that a full understanding of how pollen release occurs may often require analysis at the level of the biomechanical properties of floral structures. Fan et al. (2019, in this issue pp. 1133–1141) explore how rainwater has shaped the evolution of the pollination process in a species from a tropical monsoon environment. They show that rain-mediated pollen germination facilitates fertilization. Rebolleda-Gómez et al. (2019, in this issue pp. 1012–1020) further explore the interaction of the flower and its environment, in particular the microbial community that inhabits the flower. They raise the intriguing possibility that microbes could manipulate pollen vectors to mediate their own dispersal, with subsequent direct and indirect consequences for the evolution of plant reproductive systems. Thomson's (2019) work (in this issue pp. 1151–1159) uses supplemental pollination experiments conducted over an impressive 26 separate years, and demonstrates the challenges associated with detecting time-series changes in the level of pollinator service. Pollen is subject to a wealth of selective pressures because it serves as attractant and reward for pollinators as well as the life cycle stage that mediates fertilization for plants. Xiong et al. (2019, in this issue pp. 1142–1150) suggest that cryptic pollen colouration may enhance plant reproductive success by protecting pollen from pollen thieves– insects that consume pollen but do not contribute to pollination. Pollen is also the topic of a study by Minnaar et al. (2019, in this issue pp. 1160–1170) which draws upon developments in nanotechnology by exploiting quantum dots (atom-sized fluorophores) to label individual pollen grains in a study that elegantly demonstrates how bimodality in floral tube length leads to assortative pollination patterns and possibly reproductive isolation contributing to speciation. These studies remind us that selection is likely to have intricately shaped many aspects of pollen dispersal and receipt (Harder & Thomson, 1989). Another important area of investigation is understanding how phenotypic plasticity versus local adaptation in plant reproductive systems and life history can maintain an individual's fitness when faced with spatial and temporal variation in the environment. Both Friedman et al. (2019, in this issue pp. 1171–1183) and Ensing & Eckert (2019, in this issue pp. 1184–1200) find that phenotypic plasticity in key traits related to reproduction play a dominant role in allowing plants to grow in divergent temporal (e.g. germination in different seasons) and spatial (e.g. elevational gradients) environments. Phenotypic plasticity could play an important role in allowing plant populations to buffer the negative effects of climate change. A number of authors in this Special Issue develop evolutionary models to explore aspects of plant reproductive systems. Hodgins & Yeaman (2019, in this issue pp. 1201–1214) employed individual-based simulations of populations to show that self-fertilization influences evolutionary divergence of quantitative traits through its effect on limiting gene (pollen) flow, and that evolution of quantitative traits in self-fertilizing populations may involve a larger number of loci, each with smaller average effects compared to that in outcrossing populations. Peters & Weis (2019, in this issue pp. 1215–1228) have used a similar modelling approach to show that temporal (flowering time) and spatial structuring of gene pools can act synergistically to facilitate adaptation at small scales. Simulation modeling was used by Roux & Pannell (2019, in this issue pp. 1229–1240) to explore the interaction between migration frequency-dependent selection and drift in metapopulations, and their study reveals that a process akin to Haldane's sieve (Haldane, 1927) can counteract the tendency for lower frequency alleles that underlie phenotypes in tristylous taxa to be lost, reminding us that the genetic control of plant reproductive systems cannot be ignored in analytical approaches. Otto (2019, in this issue pp. 1241–1251) develops theory for the selective divergence of sex chromosomes, and finds that selectively-maintained polymorphisms are not expected to develop within separate 'genomic islands' outside of the sex-determining region, though suppression of recombination can allow the spread of such polymorphisms, leading to heteromorphic sex chromosomes. Cutter's (2019, in this issue pp. 1080–1094) review of theory relating to the evolution of self-fertilization reminds us of the parallels that exist with respect to mating system evolution in plants and animals and draws particular attention to the relaxation of selection that accompanies this transition, with potentially important consequences for sexual selection and the speciation process. Harder et al. (2019, in this issue pp. 1021–1034) take a novel perspective by embracing the within-plant phenotypic variation often observed for plant reproductive characteristics and considering the potential ecological and evolutionary consequences of such variation. Together these contributions underscore the continued important role of evolutionary theory for testing our intuition and pointing to new avenues of research in studies of reproductive system evolution. Looking back at the history of the field, while advances in theory of reproductive system evolution had the effect of focusing attention on experimental work directed at testing models at the population level, it soon became clear that the two approaches offer complimentary insights (Donoghue, 1989; Barrett et al., 1996). Indeed, many of the classic studies of plant reproductive biology of the mid-twentieth century took a phylogenetic and comparative perspective on the evolution of plant reproductive systems (Stebbins, 1957, 1974). Phylogenetic and comparative approaches figure prominently in several studies in this Special Issue. Zenil-Ferguson et al. (2019, in this issue pp. 1252–1265) use a new class of the binary state speciation and extinction model (Maddison et al., 2007), one that incorporates hidden states to explore the influence of ploidy and mating system on diversification rates within the Solanaceae. They find that the influence of ploidy on diversification may be best explained by its correlation with mating system, and possibly by additional unknown factors associated with the mating system. Ploidy is also the focus of the angiosperm-wide comparative analysis of Van Drunen & Husband (2019, in this issue pp. 1266–1277), which finds that polyploidy and clonality are correlated, but that there is little evidence for the hypothesis that clonality leads to the evolution of polyploidy. Costa et al. (2019, in this issue pp. 1278–1289) conducted comparative analyses of mating system transitions in Plumbaginaceae and report that the most likely common ancestor of the group was self-incompatible and monomorphic, a finding that supports one of two competing models for the evolution of heterostyly, the 'selfing avoidance' model of B. Charlesworth & D. Charlesworth (1979). Examining the breakdown of distyly within a section of Primula, Zhong et al. (2019, in this issue pp. 1290–1303) find evidence for multiple independent transitions to homostyly, accompanied by high rates of selfing and reductions in flower size and pollen output, in agreement with the notion of the selfing syndrome. Wang et al. (2019, in this issue pp. 1304–1315) extend phylogenetic methods beyond plants, examining codiversifiction of fig species, their pollinators, and parasites (gall wasps), and show that phylogenetic congruence is most pronounced for figs and their mutualistic partners. Using comparative data on hybridization together with computer simulations, Pickup et al. (2019, in this issue pp. 1035–1047) highlight the importance of mating system shifts in influencing interspecific gene flow, and thereby the nature and rate of reproductive isolation. This has important implications for the influence of mating system evolution on rates of speciation and diversification. With ever increasingly sophisticated tools for comparative studies and an expanding database for reconstructing evolutionary relationships, comparative and phylogenetic analysis of plant reproductive systems promises to figure prominently in this field to better understand the causes and macroevolutionary consequences of mating system shifts. Analyses of the genetic basis of plant reproductive systems and their correlates has enriched our understanding of how mating system and gender variation (Lande & Schemske, 1985; Couvet et al., 1998; Charlesworth & Willis, 2009; Castric et al., 2014), and more recently the tools of population genomics, have been put to the task of further revealing the evolutionary causes and consequences of the evolution of plant reproductive systems (Wright et al., 2008; Ness et al., 2010; Tsuchimatsu et al., 2017). Several papers in this Special Issue explore the underlying genetic basis of variation in reproductive systems. Some look at aspects of the genetic control of these systems. For instance, Shore et al. (2019, in this issue pp. 1316–1329) reveal that the genetic control of distyly in the genus Turnera shares some aspects of that found in Primula (hemizygosity of S-morph genes), though they find that the specific genes involved differ from those implicated in primroses. Baldwin & Schoen (2019, in this issue pp. 1330–1338) examine another class of genes implicated in mating-system evolution, in this case those underlying inbreeding depression in the self-incompatible species Leavenworthia alabamica. Hasan et al. (2019, in this issue pp. 1339–1348) examine recombination and linkage disequilibrium with respect to the mating type locus in Chlamydomonas reinhardtii and relate their findings to selection efficiency and Hill–Robertson effects. The work shows that such genes are not easy to purge and likely are numerous and of small effect. Jantzen et al. (2019, in this issue pp. 1349–1360) use a combination of transformation experiments, in vitro assays, and quantitative and population genetics methods to explore aspects of the 'selfing syndrome' in the genus Capsella, and find that while there are hotspots for mutations that are associated with scent reduction, independently-derived selfing species in the genus have undergone different genetic paths to arrive at this phenotype. Theoretical approaches such as those outlined above have stimulated many detailed population level studies that examine the evolutionary consequences of plant reproductive system variation, a trend exemplified by Ho et al. (2019, in this issue pp. 1361–1371) who used population genomic tools to reveal that populations of the highly reduced and clonally-reproducing duckweed, Spirodela polyrhiza, somewhat paradoxically harbour little genetic variation, exhibit a weak signal of purifying selection, yet show evidence of large effective population sizes. Hollister et al. (2019, in this issue pp. 1372–1380) use transcriptome sequencing and comparative population genomic analyses to show how the loss of sexual reproduction and hybridization within the genus Oenothera shapes patterns of genomic diversity and gives rise to new species. Another study in this issue (Adhikari et al., 2019, in this issue pp. 1381–1393) uses cytotype markers to examine mechanisms for the evolution of gynodioecy, and finds evidence implicating both negative-frequency dependent selection and invasion of novel male sterility genes in maintaining variation in mating systems within and between populations. Because dioecy has often evolved recently in plant populations, sex chromosomes are typically at a very early stage of formation, enabling important opportunities to investigate the genetic basis of dioecy and the evolutionary dynamics of sex chromosome and mating type evolution. Charlesworth (2019, in this issue pp. 1095–1107) reviews the possible models and evidence to date for the genetic basis of dioecy, and the dynamics leading to large-scale suppression of recombination along the sex chromosomes, highlighting growing evidence that the standard assumptions about how sex chromosomes evolve may often not hold. Delph's (2019, in this issue pp. 1075–1079) review highlights growing evidence that haploid selection during pollen competition is an important contributor to the formation and ongoing evolution of plant sex chromosomes. Li et al.'s (2019, in this issue pp. 1394–1404) experimental work in a very young sex chromosome system further suggests that early Y chromosome formation is accompanied by an absence of essential fertility genes that are maintained on the X chromosome. The study of plant reproductive systems has captured the attention and imagination of many researchers, and with good reason. Reproductive characters are closely tied to fitness and influenced by the biotic and abiotic environment, making them ideal targets for studying important ecological interactions and evolutionary change. Population-level variation in reproductive characters has clear and predictable consequences, rendering the task of theoretical modelling both satisfying and pertinent. And with the additional tool of genomics, increasingly more detail about the underlying genetic basis of reproductive systems is being revealed. It seems certain that the fusion and synthesis of ecological, evolutionary, and genetical approaches to the study of plant reproductive systems championed by Spencer Barrett and his students will continue to reveal intriguing and exciting findings in the decades to come. The research programs of DJS, MTJJ and SIW are supported by the Natural Sciences and Engineering Research Council of Canada. We wish to thank Sarah Lennon, Executive Editor, and Holly Slater, Senior Commissioning Editor at New Phytologist for their strong support and encouragement with this Special Issue. We thank Spencer Barrett for inspiring generations of researchers in the field of plant evolution and for his many years of mentorship and collaboration.

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