American Journal of Botany 100(6): 999–1001. 2013.




of Entomology, The Pennsylvania State University, University Park, Pennsylvania 16802 USA; and 3Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202 USA

• Since the time of Charles Darwin, the variation in floral characteristics and its effects on plant mating system evolution have fascinated scientists. Recent advances in the field of genetics, molecular biology, and ecology have been very effective in addressing questions regarding mechanisms and interactions underlying the evolution of plant mating systems using various model and nonmodel species. The depth of plant mating system research reflects the complexity and diversity seen in nature, ranging from self-compatible hermaphroditic flowers to separate sexed individuals. Further, the mechanisms involved in the evolution of plant mating systems are much more diverse and differ even among closely related species. Here, as a special section, we present a suite of original papers that range from theoretical modeling to multiyear field research that address different factors affecting plant mating systems, and their effects on shaping interactions between plants, insects, and their environment. Key words: dioecy; inbreeding depression; plant hormones; hybridization; heterospecific pollen: floral morphology.

The diversity seen in the sexual mating systems of angiosperms is a continued source of interest for botanists and evolutionary biologists. Although variation in plant mating systems has inspired research for centuries, experimentation in this area has exploded in the last decade, thanks, in part, to ever-increasing and affordable technologies. Scientists have been able to tease out components of mating system evolution using tools derived from various disciplines from molecular phylogenetics to chemical ecology. Today, the area of plant mating systems encompasses a wide and diverse range of specialties. These include empirical field and laboratory studies, phylogenetics, and theoretical modeling. With such diverse specialties and the volume of work being produced, special issues/sections that bring together various aspects of mating system evolution serve a crucial role in unifying the field. Since the time of Darwin (1877), variation and evolution of flower structure and function have remained as a central focus of evolutionary biology. This is primarily because flower
1 Manuscript received 29 April 2013; revision accepted 9 May 2013. The authors sincerely thank AJB staff for the tremendous amount of work and patience to get this issue into shape. We cannot imagine this special section to be completed without the support and efforts of Amy McPherson, Managing Editor; Sophia Balcomb, Content Editor; and Richard Hund, Production Editor, of AJB. We also thank all the authors and anonymous reviewers for the timely submissions, revisions, and reviews. Additionally, we thank Judy Jernstedt, Editor-in-Chief, for giving us the opportunity to put together a symposium and this special section. Finally, we thank the Botanical Society of America Ecological and Genetics sections as well as the Torrey Botanical Society for funding the 2012 BSA symposium, which served as the catalyst whose result is this special section. R.R.K. and J.P.S. contributed equally to this work. 4 Author for correspondence (e-mail:


morphology and phenology directly affect essential population genetic and ecological parameters such as mate choice, fecundity, inbreeding coefficients, ecological plasticity, speciation, and interspecific competition and cooperation. Therefore, studies that track the role of floral evolution in adaptation and speciation should theoretically encompass all these aspects. Clearly, a complete exploration of all of these factors in a single experimental design is impossible. Consequently, studies in floral evolution and reproductive strategies tend to coalesce in separate foci. For example, the effects of reproductive strategies on inbreeding and subsequent inbreeding depression have been considered a major driving factor in plant mating system evolution (Charlesworth and Charlesworth, 1978). Alternatively, reproductive specializations that increase intrinsic fecundity or decrease costs to viability and survivorship in an ecological context can also be important factors in selective evolution of mating systems. Other areas of mating system evolution studies focus on the indirect effects of habitat fragmentation (Mannouris and Byers, 2013), pleiotropy (Jordan and Otto, 2012), and prezygotic isolation to prevent hybridization (Ludwig et al., 2013). Thus, mating system evolution in plants is clearly a vibrant and thriving discipline. In an attempt to bring a number of similarly focused studies together and to report on emerging trends in the field, we have put together this special section featuring 10 papers that highlight different influences affecting the evolution of plant mating systems. The issue includes original papers written by a diverse group of scientists ranging from molecular biologists to ecologists. While each concentrates on a narrow aspect in the spectrum of plant mating system studies, the thematic overlaps among the papers strikingly illustrate the complexity and the interconnected effects of floral evolution. Broadly speaking, variations in mating systems have short-term or ecological effects on individuals within defined habitats and long-term or evolutionary effects on populations over time. The continuous

American Journal of Botany 100(6): 999–1001, 2013; © 2013 Botanical Society of America


The evolution of derived traits. The notion that environmentally induced phenotypes can become assimilated into the genome has historically been controversial. and ecological costs due to inbreeding or outcrossing. they provide valuable insights into how bat pollination/foraging can affect pollen exchange. On an ecological scale. and the loss of this plasticity results in a reversion to predominantly hermaphroditic flowers. low susceptibility to deleterious heterospecific pollen. This paper directly examines the cost of inbreeding in terms of constitutive and induced expression of structural defenses. herbivore-damaged. Quesada et al. the primary factors that affect and are affected by plant mating systems are spatial pollinator and mate availability. The authors examine how differential heterospecific pollen reception results in various hybridization rates and how hybridization can select for selfing through low fitness hybrids. A second outcome of heterospecific pollen deposition. Due to the lack of genetic markers and other logistical constraints. Habitat fragmentation causes spatial isolation of individuals and populations and results in significant effects on population genetic substructuring. authors of the first paper of the special section. tackle the first of these ecological problems. Here. The authors found that specialist herbivory and mechanical wounding differentially induced defenses. and their interactions with floral traits in natural communities. their various interactions and bidirectional influences have received much less attention. their pollination biology. Their observations suggest that dioecy is more common in parasitic plants than nonparasitic plants. This correlation suggests that dimorphic traits between the phenotypes are subjected to and respond to multiple changes simultaneously. Both presence and extent of phenotypic variation were used in conjunction with phylogenetic analysis to develop a model for the phenotypic evolution of sexual expression in Solanum. This study provides highly suggestive evidence for the process of . which were significantly impaired by inbreeding. Goodwillie and Ness (2013) examine the relationship between heterospecific pollen reception and mating system using the self-incompatible species Leptosophon androaceus and the closely related. 100 flux between these scales of effects is a hallmark of these collected papers and illuminates the fundamental importance of plant reproductive system evolution. Carried out over 4 years of fieldwork. Using pollinator data collected from multiple field stations and by incorporating recent advances in phylogenetics. resource allocation toward male and female sexual functions and the associated fitness benefits have been well documented as a driver of mating system evolution in flowering plants. has been well studied in a variety of species. Diggle and Miller (2013) examine the relationship between floral plasticity and mating system evolution using phylogenetic comparisons in 14 species of Solanum. and mechanically damaged plants to examine costs associated with inbreeding. An alternative to the evolution of fixed or dimorphic changes in reproductive systems in response to environmental constraints is the strategy of phenotypic plasticity by which an individual can develop transient or reversible changes that are beneficial in fluctuating environments. For example. Phenotypic variation was encouraged in each of the study species through the manipulation of individual resource availability. reproductive strategies among them. Bellot and Renner (2013) address questions about parasitic angiosperm lineages. They propose a rubric of traits that are associated with high vs. primarily caused by pollen reduction. area of botanical research. The results suggest that the interaction effects are complex but that early selfing may be selected for as a means of avoiding hybridization. reproductive biology of parasitic angiosperms is a fascinating.1000 AMERICAN JOURNAL OF BOTANY [Vol. Ashman and Arceo-Gómez (2013) use an extensive literature-driven meta-analysis to dissect the morphological and mating strategy traits involved in heterospecific pollen deposition and receipt. especially in perennial tree species. Heterospecific pollen (HP) deposition can result in interference of conspecific pollination and fertilization or hybridization. In contrast to low effective pollen abundance in fragmented communities. this study addresses the topic experimentally with detailed methods and a combination of analytical tools. (2013) build on this concept by examining differential biomass allocation using both morphological and fitness traits in two gynodioecious species. These in turn can result in changes in the flexibility to respond to environmental stresses. Differential costs lend support for selection toward an outcrossing system and/or the prevalence of a mixed mating system—a crucial step required to support current theory. Sakai et al. (2013). asking whether some of the major fitness variables differ among disturbed and nondisturbed habitats over multiple years of growth. giving rise to questions on phylogenetic and mechanistic influences on the mating system evolution of parasites. and their sexual system. However. Quesada et al. the morphological and biomass traits commonly examined in sex allocation models are highly correlated. In addition. which is thought to be en route to dioecy from gynodioecy. Their comprehensive analyses suggest that in a genus such as Schiedea. including genetic differentiation of populations and increased inbreeding. (2013) specifically target this question by using the tropical tree species Ceiba aesculifolia. This study will surely attract scientists who are interested in how mating systems evolve around pollinators. this study adds to the few studies that combine pollination biology and genetics to understand how habitat fragmentation can affect mating system evolution in perennials. Apodanthaceae. (2013) examine inbreeding and herbivore resistance in the perennial weed Solanum carolinense. Schiedea salicaria and Schiedea adamantis. hybridization. Stellate trichomes and internode spines were measured on control. The lack of pollinator data and the absence of phylogeny-based reviews are some of the factors that have been hampering progress in this field. a common population biology process. From the adaptive ecological perspective. highly selfing Leptosophon jepsonii. competition and interference in pollination efficiency among conspecific and heterospecific individuals. Results suggest that in Solanum phenotypic plasticity is ancestral. although understudied. Kariyat et al. multiple-year field studies addressing fragmentation and its interactions with pollinators and mating system evolution are limited. can reflect strong adaptive components or can be constrained by canalizing genetic limitations that appear to be phylogenetically associated. an excess of pollen within communities can lead to pollen interference or hybridization. Coflowering of different species primarily drives pollinator sharing. and their fitness consequences. The authors also provide an extensive review of the reproductive biology of an important parasitic plant family. Despite implications of a more complex relationship between mating system and hybridization. Their results suggest that relatedness among progeny increases in disturbed habitats. Mating systems not only affect genetic diversity on the population level but also on the individual level through inbreeding and increased homozygosity.

SAKAI. RICH. C.—INTRODUCTION: EVOLUTION OF PLANT MATING SYSTEMS 1001 assimilation and the association of floral plasticity with mating system evolution. Carr (2013) re-examines the interplay between genetics and ecology underlying floral form and function. STEPHENSON. UK. AND S. D. GOLENBERG. MAXWELL. E. DJORDJEVIC. Hormonal interactions and gene regulation can link monoecy and environmental plasticity to the evolution of dioecy in plants. discrete phenomena. American Journal of Botany 100: 1083–1094.June 2013] KARIYAT ET AL. Breeding systems. M. as special section editors. The different forms of flowers on plants of the same species. Biological Journal of the Linnean Society 108: 55–67. ROSAS. 1978. SÁNCHEZ-MONTOYA. and papers with data collected from both field and laboratory studies. G.. HISCOCK. The paper clearly establishes why interdisciplinary and multidimensional approaches are required to study mating systems and thereby to understand plant evolution. D. we are excited to present a set of papers that aim to provide readers with a comprehensive collection of current topics in the field of plant mating system evolution. The authors also call for new studies specifically targeting individual genes involved in sex determination to address the major question of single gene effects. C. AND J. The impact of habitat fragmentation on fitness-related traits in a native prairie plant. L. HOUSTON. bringing together a wide variety of researchers broadly interested in plant mating systems and reproduction. the result is a set of invasion criteria that is substantially less strict than previously suggested. M. MANNOURIS. T. C. 2013. Developmental plasticity. A. Ceiba aesculifolia (Malvaceae: Bombacoideae). American Journal of Botany 100: 1022–1037. R. dioecy. HERRERIAS-DIEGO. Y. CARR. R. CULLEY. A model for the evolution of dioecy and gynodioecy. C. ROBERTSON. L. genetic models and functional genomics studies that accurately predict sex determination in flowering plants are still lacking. Such genetic/ developmental models may be the basis of developmental tradeoffs such as those presented in this collection of papers. M. London.. Furthermore.. AND D. Long-term effects of habitat fragmentation on mating patterns and gene flow of a tropical dry forest tree. J. American Journal of Botany 100: 1050–1060. P. American Journal of Botany 100: 1002–1013. re-examines the evolution of dioecy using a dynamic simulation. K. environmental sex determination. R. NESS. T. rather than being distinct. and dispersal patterns are well studied in their own right. American Journal of Botany 100: 1095–1101. M. We anticipate that this set of papers will serve as a vertex. S. FREEMAN. JORDAN. and the evolutionary diversification of sexual expression in Solanum. by Sinclair et al. 2012. specialization. Additionally. The next paper in this special section. QUESADA. Evolution 66: 957–972. BALOGH. M. DIGGLE. WEST. C. CAMPBELL. P. Constitutive and herbivore-induced structural defenses are compromised by inbreeding in Solanum carolinense (Solanaceae). Consanguineous mating. LUDWIG. MESCHER. Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. KARIYAT.. S. G. Y. GOODWILLIE. G. 2013. C. Inbreeding depression. primarily due to the dearth of comprehensive reviews on the factors that affect sex determination. BELLOT. 2013. MILLER. CHARLESWORTH. American Journal of Botany 100: 1061–1070. and sexual plasticity as part of an evolutionary continuum. 2013. LOBO. AND R.or androdioecious species. AND J. DUNBAR-WALLIS. DARWIN. A. CEROVIC. but when considered together. R. Often environmental sex determination and genetic sex determination are treated as two distinct processes. T. John Murray. M. D. Annals of Botany 111: 563–575. S. S. American Journal of Botany 100: 1014–1021. 2013. Using the special section papers as a template. G. the authors put forward a genetic model that addresses how gene networks interact with each other and influence floral sex expression. S.. AND D. This special section concludes with a commentary by Carr (2013). AND A. OTTO. 2013. AND G. Predictions for alternative genomic evolutionary effects of the different models of sex determination are presented that can be tested through comparative genomic studies.. genetic assimilation. HARRIS.. MORASKI. Measure for measure: Comparing morphological and biomass traits for sex allocation in two gynodioecious species. AND N. Perhaps looking at a familiar topic through a new lens will ignite new questions and lead to exciting and novel future research. AND A. WELLER. W.. B. AND S. this model focuses on the importance of multiple variable interactions as a means to obtain invasion conditions representative of patterns commonly observed in nature. American Journal of Botany 100: 1071–1082. AND D.. and formats. The results support not only the wide phylogenetic range of dioecious species. S. but also the variability in population dynamics (including population sex ratio) that are seen among the various intermediate and mixed gender populations such as found in gyno. This new model attempts to unify processes that lead to monoecy. A. hybridization and continuing evolution in Avon Gorge Sorbus. Pollination and mating systems of Apodanthaceae and the distribution of reproductive traits in parasitic angiosperms. (2013).-L. American Journal of Botany 100: 1038–1049. which is often omitted from such models yet is shown here to be an important facilitator of the evolution of dioecy when coupled with even moderate levels of inbreeding depression. E. This model also considers the effects of mating between close relatives. on the basis of various genes involved in phytohormone pathways and ancillary signaling networks. CHARLESWORTH. A. AND S. 1877. Environmentally induced phenotypic plasticity has been a persistent problem in the study of the genetics and evolution of sexual differentiation and mating systems. 2013. 2013.. . To conclude. ARCEO-GÓMEZ. M. Special care was taken to incorporate papers from various subdisciplines. R. Based on a two-mutation assumption. We were fortunate to be able to include theoretical models. C. K. American Naturalist 112: 975–997. ANDRES.. Chamaecrista fasciculata (Fabaceae). Interactions of hybridization and mating systems: A case study in Leptosiphon (Polemoniaceae). J. AGUILAR. RENNER.. C.. 2013. LITERATURE CITED ASHMAN. 2013. C. M. K. M. reviews. BYERS. F. American Journal of Botany 100: 1102–1104. P. A. A multi-dimensional approach to understanding floral function and form. SINCLAIR. DE MORAES. 2013. and the environment: How multiple variable interactions affect the evolution of dioecy. R. 2013. G. J. P. Functional pleiotropy and mating system evolution in plants: Frequency-independent mating. compensation. Golenberg and West (2013) tackle this issue by extensively reviewing the literature on sex determination and focusing on how hormonal regulation and environmental stimuli affect sex determination and sexual plasticity.

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