American Journal of Botany 100(6): 9991001. 2013.

SPECIAL INVITED PAPEREVOLUTION OF PLANT MATING SYSTEMS

FOLLOWING DARWINS TRAIL: INTERACTIONS AFFECTING THE

EVOLUTION OF PLANT MATING SYSTEMS1

RUPESH R. KARIYAT2, JORDAN P. SINCLAIR3,4 AND EDWARD M. GOLENBERG3

2Department

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 oral characteristics and its effects on plant mating system evolution have fascinated scientists. Recent advances in the eld 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 reects the complexity and diversity seen in nature, ranging from self-compatible hermaphroditic owers 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 eld 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; heterospecic pollen: oral 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 eld 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 eld. Since the time of Darwin (1877), variation and evolution of ower structure and function have remained as a central focus of evolutionary biology. This is primarily because ower
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: al8577@wayne.edu)

doi:10.3732/ajb.1300157

morphology and phenology directly affect essential population genetic and ecological parameters such as mate choice, fecundity, inbreeding coefcients, ecological plasticity, speciation, and interspecic competition and cooperation. Therefore, studies that track the role of oral 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 oral 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 eld, we have put together this special section featuring 10 papers that highlight different inuences 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 oral evolution. Broadly speaking, variations in mating systems have short-term or ecological effects on individuals within dened habitats and long-term or evolutionary effects on populations over time. The continuous

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ux between these scales of effects is a hallmark of these collected papers and illuminates the fundamental importance of plant reproductive system evolution. On an ecological scale, the primary factors that affect and are affected by plant mating systems are spatial pollinator and mate availability, competition and interference in pollination efciency among conspecic and heterospecic individuals, and ecological costs due to inbreeding or outcrossing. Quesada et al. (2013), authors of the rst paper of the special section, tackle the rst of these ecological problems. Habitat fragmentation causes spatial isolation of individuals and populations and results in signicant effects on population genetic substructuring, including genetic differentiation of populations and increased inbreeding. Due to the lack of genetic markers and other logistical constraints, multiple-year eld studies addressing fragmentation and its interactions with pollinators and mating system evolution are limited, especially in perennial tree species. Quesada et al. (2013) specically target this question by using the tropical tree species Ceiba aesculifolia, asking whether some of the major tness variables differ among disturbed and nondisturbed habitats over multiple years of growth. Their results suggest that relatedness among progeny increases in disturbed habitats, primarily caused by pollen reduction. In addition, they provide valuable insights into how bat pollination/foraging can affect pollen exchange. Carried out over 4 years of eldwork, 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. In contrast to low effective pollen abundance in fragmented communities, an excess of pollen within communities can lead to pollen interference or hybridization. Coowering of different species primarily drives pollinator sharing, a common population biology process. Heterospecic pollen (HP) deposition can result in interference of conspecic pollination and fertilization or hybridization. Ashman and Arceo-Gmez (2013) use an extensive literature-driven meta-analysis to dissect the morphological and mating strategy traits involved in heterospecic pollen deposition and receipt, and their tness consequences. They propose a rubric of traits that are associated with high vs. low susceptibility to deleterious heterospecic pollen. This study will surely attract scientists who are interested in how mating systems evolve around pollinators, and their interactions with oral traits in natural communities. A second outcome of heterospecific pollen deposition, hybridization, has been well studied in a variety of species. Despite implications of a more complex relationship between mating system and hybridization, their various interactions and bidirectional inuences have received much less attention. Here, Goodwillie and Ness (2013) examine the relationship between heterospecic pollen reception and mating system using the self-incompatible species Leptosophon androaceus and the closely related, highly selng Leptosophon jepsonii. The authors examine how differential heterospecic pollen reception results in various hybridization rates and how hybridization can select for selng through low tness hybrids. The results suggest that the interaction effects are complex but that early selfing may be selected for as a means of avoiding hybridization. The evolution of derived traits, reproductive strategies among them, can reect strong adaptive components or can be constrained by canalizing genetic limitations that appear to be phylogenetically associated. For example, reproductive biology of parasitic angiosperms is a fascinating, although understudied,

area of botanical research. The lack of pollinator data and the absence of phylogeny-based reviews are some of the factors that have been hampering progress in this eld. Using pollinator data collected from multiple eld stations and by incorporating recent advances in phylogenetics, Bellot and Renner (2013) address questions about parasitic angiosperm lineages, their pollination biology, and their sexual system. The authors also provide an extensive review of the reproductive biology of an important parasitic plant family, Apodanthaceae. Their observations suggest that dioecy is more common in parasitic plants than nonparasitic plants, giving rise to questions on phylogenetic and mechanistic inuences on the mating system evolution of parasites. From the adaptive ecological perspective, resource allocation toward male and female sexual functions and the associated tness benets have been well documented as a driver of mating system evolution in owering plants. Sakai et al. (2013) build on this concept by examining differential biomass allocation using both morphological and tness traits in two gynodioecious species, Schiedea salicaria and Schiedea adamantis. Their comprehensive analyses suggest that in a genus such as Schiedea, which is thought to be en route to dioecy from gynodioecy, the morphological and biomass traits commonly examined in sex allocation models are highly correlated. This correlation suggests that dimorphic traits between the phenotypes are subjected to and respond to multiple changes simultaneously. Mating systems not only affect genetic diversity on the population level but also on the individual level through inbreeding and increased homozygosity. These in turn can result in changes in the exibility to respond to environmental stresses. Kariyat et al. (2013) examine inbreeding and herbivore resistance in the perennial weed Solanum carolinense. This paper directly examines the cost of inbreeding in terms of constitutive and induced expression of structural defenses. Stellate trichomes and internode spines were measured on control, herbivore-damaged, and mechanically damaged plants to examine costs associated with inbreeding. The authors found that specialist herbivory and mechanical wounding differentially induced defenses, which were signicantly impaired by inbreeding. Differential costs lend support for selection toward an outcrossing system and/or the prevalence of a mixed mating systema crucial step required to support current theory. An alternative to the evolution of xed 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 benecial in uctuating environments. Diggle and Miller (2013) examine the relationship between oral plasticity and mating system evolution using phylogenetic comparisons in 14 species of Solanum. The notion that environmentally induced phenotypes can become assimilated into the genome has historically been controversial. However, this study addresses the topic experimentally with detailed methods and a combination of analytical tools. Phenotypic variation was encouraged in each of the study species through the manipulation of individual resource availability. 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. Results suggest that in Solanum phenotypic plasticity is ancestral, and the loss of this plasticity results in a reversion to predominantly hermaphroditic owers. This study provides highly suggestive evidence for the process of

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assimilation and the association of oral plasticity with mating system evolution. Environmentally induced phenotypic plasticity has been a persistent problem in the study of the genetics and evolution of sexual differentiation and mating systems. Often environmental sex determination and genetic sex determination are treated as two distinct processes. Furthermore, genetic models and functional genomics studies that accurately predict sex determination in owering plants are still lacking, primarily due to the dearth of comprehensive reviews on the factors that affect sex determination. 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. Additionally, on the basis of various genes involved in phytohormone pathways and ancillary signaling networks, the authors put forward a genetic model that addresses how gene networks interact with each other and inuence oral sex expression. Such genetic/ developmental models may be the basis of developmental tradeoffs such as those presented in this collection of papers. This new model attempts to unify processes that lead to monoecy, dioecy, environmental sex determination, and sexual plasticity as part of an evolutionary continuum, rather than being distinct, discrete phenomena. Predictions for alternative genomic evolutionary effects of the different models of sex determination are presented that can be tested through comparative genomic studies. The authors also call for new studies specically targeting individual genes involved in sex determination to address the major question of single gene effects. The next paper in this special section, by Sinclair et al. (2013), re-examines the evolution of dioecy using a dynamic simulation. Based on a two-mutation assumption, this model focuses on the importance of multiple variable interactions as a means to obtain invasion conditions representative of patterns commonly observed in nature. Inbreeding depression, compensation, and dispersal patterns are well studied in their own right, but when considered together, the result is a set of invasion criteria that is substantially less strict than previously suggested. The results support not only the wide phylogenetic range of dioecious species, 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- or androdioecious species. This model also considers the effects of mating between close relatives, 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. This special section concludes with a commentary by Carr (2013). Using the special section papers as a template, Carr (2013) re-examines the interplay between genetics and ecology underlying oral form and function. The paper clearly establishes why interdisciplinary and multidimensional approaches are required to study mating systems and thereby to understand plant evolution. To conclude, as special section editors, we are excited to present a set of papers that aim to provide readers with a comprehensive collection of current topics in the eld of plant mating system evolution. Special care was taken to incorporate papers from various subdisciplines, and formats. We were fortunate to

be able to include theoretical models, reviews, and papers with data collected from both eld and laboratory studies. We anticipate that this set of papers will serve as a vertex, bringing together a wide variety of researchers broadly interested in plant mating systems and reproduction. Perhaps looking at a familiar topic through a new lens will ignite new questions and lead to exciting and novel future research.

LITERATURE CITED
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