Plant Mating Systems

The remarkable diversity of mating patterns and sexual systems in flowering plants has fascinated evolutionary biologists for more than a century. Enduring questions about this topic include why sexual polymorphisms have evolved independently in over 100 plant families, and why proportions of self- and cross-fertilization often vary dramatically within and among populations. Important new insights concerning the evolutionary dynamics of plant mating systems have built upon a strong foundation of theoretical models and innovative field and laboratory experiments. However, as the pace of advancement in this field has accelerated, it has become increasingly difficult for researchers to follow developments outside their primary area of research expertise.

In this issue we highlight three important themes that span and integrate different subdisciplines: the changes in morphology, phenology, and physiology that accompany the transition to selfing; the evolutionary consequences of pollen pool diversity in flowering plants; and the evolutionary dynamics of sexual polymorphisms. We also highlight recent developments in molecular techniques that will facilitate more efficient and cost-effective study of mating patterns in large natural populations, research on the dynamics of pollen transport, and investigations on the genetic basis of sexual polymorphisms.

Contents

Mathilde Dufay and Emmanuelle Billard
How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species.

Theoretically, females should be able to coexist with hermaphrodites only if they benefit from a reproductive advantage. By reviewing and analysing data published on 48 species, Dufay and Billard (pp. 505–519) show that this expectation is usually true; however, the magnitude of the advantage shows considerable variation among, and sometimes within, species, and its proximal causes vary from one species to another. They suggest that reduced selfing may not be the major cause of the occurrence of female advantage, and thus of the maintenance of gynodioecy.

Glenda Vaughton and Mike Ramsey
Gender plasticity and sexual system stability in Wurmbea

Gender plasticity in hermaphrodites is proposed to influence the evolution of separate sexes. Vaughton and Ramsey (pp. 521–530) characterize gender plasticity in hermaphrodites and unisexuals under different resource conditions in two Wurmbea species with sexual systems ranging from cosexuality to dioecy. They find that hermaphrodites produce fewer perfect flowers, but not staminate flowers, when resources are reduced; unisexuals are unaffected. This study highlights the importance of interactions between the environment and hermaphrodite gender expression for the stability of sexual systems.

Rachel B. Spigler and Tia-Lynn Ashman
Gynodioecy to dioecy: are we there yet?

The transition from combined sexes (hermaphroditism) to separate sexes (dioecy) is a fundamental one in flowering plants. Evidence and subsequent understanding of how females invade and establish in hermaphroditic populations at the beginning of the ‘gynodioecy–dioecy pathway’ is rich compared to that for later stages, wherein males invade and supplant hermaphrodites. Spigler and Ashman (pp. 531–543) review existing evidence for the latter part of the pathway and discuss how major ecological factors can influence these dynamics.

Junmin Li, Matthew H. Koski, and Tia-Lynn Ashman
Functional characterization of gynodioecy in Fragaria vesca ssp. bracteata (Rosaceae)

Gynodioecy is a phylogenetically widespread sexual system where females coexist with hermaphrodites. Because dioecy can arise from gynodioecy, characterization of gynodioecy in close relatives of dioecious and subdioecious species can provide insights into this transition. Li et al. (pp. 545–552) report functional evidence of gynodioecy in Fragaria vesca ssp. bracteata, the only diploid Fragaria species that is not hermaphroditic. While the sex morphs allocate similarly to reproduction, hermaphrodites are highly selfing in the field and their progeny are less likely to germinate, suggesting inbreeding depression as a potential driver of female maintenance. Compared to subdioecious and dioecious congeners, sexual dimorphism in this gynodioecious species is less pronounced.

Jeremiah W. Busch and Lynda F. Delph
The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization

Many possible mechanisms drive the evolutionary trend from outcrossing to selfing, but most research has focused upon the transmission advantage of selfing and its ability to provide reproductive assurance when cross-pollination is uncertain. Busch and Delph (pp. 553–562) discuss the shared conceptual framework of these ideas and their empirical support that is emerging from tests of their predictions over the last 25 years. They conclude that although reproductive assurance appears likely as a leading factor facilitating the evolution of selfing, studies must account for both seed and pollen discounting to adequately test this hypothesis.

Jeffrey D. Karron and Randall J. Mitchell
Effects of floral display size on male and female reproductive success in Mimulus ringens

The number of flowers blooming simultaneously on a Mimulus ringens plant often varies markedly within populations. By combining floral display manipulations with unambiguous paternity assignment, Karron and Mitchell (pp. 563–570) demonstrate that an increase in display size leads to a dramatic reduction in outcross siring success per flower, but only a modest increase in selfing. Their results suggest that pollen discounting may play a critical role in the evolution of floral display strategies.

Susan Kalisz, April Randle, David Chaiffetz, Melisa Faigeles, Aileen Butera, and Craig Beight
Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed-mating genus Collinsia

Collinsia is a genus of self-compatible mixed-mating species that differ markedly in floral morphological and developmental traits associated with mating system variation. Kalisz et al. (pp. 571–582) find that the presence or absence of dichogamy is diagnostic of selfing and outcrossing syndromes. However, species in both syndrome groups express equal and high rates of autonomous selfing in the absence of pollinators and highly variable selfing rates in nature. This points to the critical influence of the pollination environment and the lability of dichogamy for mating system evolution of this clade.

Christopher T. Ivey and David E. Carr
Tests for the joint evolution of mating system and drought escape in Mimulus

Self-fertilization may be directly selected or may evolve indirectly through selection on other traits with which it is correlated. Ivey and Carr (pp. 583–598) test the hypothesis that selfing in the genus Mimulus evolved jointly with traits that allow plants to avoid exposure to seasonal drought. Under field and controlled drought conditions they measure phenotypic and genetic responses of drought escape and mating system traits. Although some measured traits are inconsistent with the hypothesis, several plastic responses to soil moisture treatments support the idea that taxonomic divergence could have been facilitated by plasticity in flowering time and selfing, and further study is warranted.

Sara R. Dart, Karen E. Samis, Emily Austen, and Christopher G. Eckert
Broad geographic covariation between floral traits and the mating system in Camissoniopsis cheiranthifolia (Onagraceae): multiple stable mixed mating systems across the species’ range?

Plants vary widely in the extent to which seeds are produced via self-fertilization vs. outcrossing, but whether there are distinct stable endpoints of mating system evolution is unresolved. Dart et al. (pp. 599–611) analyse geographic variation in floral traits together with genetic mating system estimates for the coastal dune endemic Camissoniopsis cheiranthifolia (Onagraceae) and show that the transition to complete selfing has not occurred even though the species appears to possess the required genetic capacity. Instead they hypothesize that outcrossing populations in this species have evolved to different stable states of mixed mating.

Donald A. Levin
Mating system shifts on the trailing edge

The trailing edges of species’ ranges are becoming a subject of increasing interest as the environment changes due to global warming. In this review, Levin (pp. 613–620) notes that small populations on the trailing edge will probably experience low levels of cross-pollination, and hence individuals that are self-compatible and are capable of self-pollination will be at an advantage. By virtue of the reproductive assurance it confers, systematic degradation of the environment will thus favour the elevation of self-fertility, which may arise in the short term through developmental responses to stress or in the longer term by changes in the self-incompatibility locus or genes that affect the behaviour of this locus. However, selfing will also lead to substantial reductions in genetic diversity, which may render adaptation unlikely.

C. J. Murren and M. R. Dudash
Variation in inbreeding depression and plasticity across native and non-native field environments

Inbreeding depression and plasticity have been hypothesized to be critical to initial establishment success of populations in novel environments. Comparing the performance of outcrossed and inbred lines of Mimulus guttatus across native and novel field sites, Murren and Dudash (pp. 621–632) find that inbreeding depression and phenotypic plasticity vary among field sites. Outcrossed offspring generally outperform selfed offspring, yet in the native-novel site self-progeny perform better or equally well as outcross progeny. Evidence is detected for greater plasticity to novel sites and an interaction between inbreeding and plasticity, suggesting the importance of both responses outside a species’ currently inhabited range.

P.-O. Cheptou
Clarifying Baker’s Law

Baker’s Law states that colonization by self-compatible organisms is more likely to be successful than colonization by self-incompatible organisms because of the ability of self-compatible organisms to produce offspring without pollination agents. Cheptou (pp. 633–641) reviews data and concepts relating to Baker’s Law and concludes that it is not totally compatible with mating system models based on a population genetic perspective, which assess ‘fitness’ in terms of genes transmitted rather than from the more demographic view taken by Baker. There is a need to characterize colonization/extinction dynamics, i.e. metapopulation scenarios, in order to interpret selection processes.

Andrew G. Young, Linda M. Broadhurst, and Peter H. Thrall
Non-additive effects of pollen limitation and self-incompatibility reduce plant reproductive success and population viability

Pollen limitation and loss of self-incompatibility genotypes can both act independently to reduce seed set in fragmented landscapes. Young et al. (pp. 643–653) use a simulation model to examine effects of pollen limitation and loss of self-incompatibility alleles on the reproductive success and population viability of a short-lived perennial herb. They find that population decline may occur more rapidly than expected when pollination probabilities drop below 25 % and S alleles are fewer than 20 due to non-additive interactions. These are likely to be common conditions experienced by plants in small populations in fragmented landscapes.

V. Ferrero, J. Arroyo, S. Castro, and L. Navarro
Unusual heterostyly: style dimorphism and self-incompatibility are not tightly associated in Lithodora and Glandora (Boraginaceae)

Heterostyly is characterized by the reciprocal position of stamens and stigmas in different flower morphs, and is usually associated with an incompatibility system that prevents selfing and intra-morph cross-fertilization. Ferrero et al. (pp. 655–665) examine incompatibility systems in Lithodora and Glandora (Boraginaceae), which have different stylar polymorphisms, and reconstruct a phylogeny of these genera and related species. They conclude that stylar polymorphism and the incompatibility system appear to have evolved independently in this group of plants, which contrasts with the orthodox view that there is strong linkage between these reproductive traits.

Caroli de Waal, Bruce Anderson, and Spencer C. H. Barrett
The natural history of pollination and mating in bird-pollinated Babiana (Iridaceae)

Bird pollination has originated in many angiosperm lineages but little is known about the mating biology of sunbird-pollinated plants. De Waal et al. (pp. 667–679) investigate the floral ecology of four species of Babiana (Iridaceae) endemic to the Cape region of South Africa. This group is of special interest because several possess the most specialized bird perch known in the plant kingdom. Using genetic markers they demonstrate self-fertilization in all populations, indicating that pollinator specialization is not always associated with cross-fertilization, as is often assumed.

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