Evolution Of Plant Mating Systems Research Articles

Pollen limitation influences the divergences in mating system and floral traits between two sympatric Halenia species

Abstract The mating systems and floral traits often among relatives of hermaphroditic plants can exhibit considerable diversity. This diversity can be influenced by the evolution of selfing and associated floral traits as a form of reproductive assurance when pollen limitation results from insufficient pollinator availability. To explore whether the degree of pollen limitation primarily drives differences in mating systems and floral traits, we conducted a comprehensive study involving two closely related species, Halenia elliptica and H. grandiflora, in three sympatric sites. We investigated floral characteristics, pollinator visitation, pollen limitation, autonomous selfing ability, reproductive assurance and mating system in studied populations. Our findings show that H. elliptica produces smaller flowers and less nectar production than H. grandiflora, making it less attractive to pollinators. Compared with H. grandiflora, H. elliptica experienced more severe outcross pollen limitation, but compensates with a higher capacity for autonomous selfing, ensuring seed production under natural conditions. Moreover, significant differences in mating systems were detected between them, with H. elliptica exhibiting a higher selfing rate than H. grandiflora across all studied sympatric populations. These differences are also reflected in variations in herkogamy and dichogamy. Our study suggested that the degree of outcross pollen limitation impacts the divergence in mating systems and floral traits between sympatric closely related species, offering valuable insights into the evolution of plant mating systems and floral traits.

Pollinator foraging tactics have divergent consequences for the mating system of a tropical plant.

Resolving the consequences of pollinator foraging behaviour for plant mating systems is a fundamental challenge in evolutionary ecology. Pollinators may adopt particular foraging tactics: complete trapline foraging (repeated movements along a fixed route), sample-and-shift trapline foraging (a variable route that incorporates information from previous experiences) and territorial foraging (stochastic movements within a restricted area). Studies that integrate these pollinator foraging tactics with plant mating systems are generally lacking. We investigate the consequences of particular pollinator foraging tactics for Heliconia tortuosa. We combine parentage and sibship inference analysis with simulation modelling to: estimate mating system parameters; infer the foraging tactic adopted by the pollinators; and quantify the impact of pollinator foraging tactics on mating system parameters. We found high outcrossing rates, ubiquitous multiple paternity and a pronounced departure from near-neighbour mating. We also found that plants repeatedly receive pollen from a series of particular donors. We infer that the pollinators primarily adopt complete trapline foraging and occasionally engage in sample-and-shift trapline foraging. This enhances multiple paternity without a substantial increase in near-neighbour mating. The particular pollinator foraging tactics have divergent consequences for multiple paternity and near-neighbour mating. Thus, pollinator foraging behaviour is an important driver of the ecology and evolution of plant mating systems.

Isolation and characterization of microsatellites markers in Centaurium grandiflorum ssp. boissieri.

Estimating outcrossing/selfing rates and characterizing genetic diversity with microsatellite markers are crucial to understanding the evolution of plant mating systems. We developed, optimized and characterized eight new primer pairs for Centaurium grandiflorum ssp. boissieri and transferred them to three subspecies of Centaurium quadrifolium. Two SSR loci were transferred from Sabatia campestris to the four Centaurium taxa. Polymorphisms, He, Ho and H-W deviations were estimated in two populations of C. grandiflorum ssp. boissieri and in seven individuals each of C. quadrifolium ssp. barrelieri, C. quadrifolium ssp. parviflorum and C. quadrifolium ssp. quadrifolium. A total of 80 individuals was used in these experiments. The number of polymorphic loci varied among species from one to ten. A total of 127 alleles was scored. The average number of alleles per locus was 12.7. He was higher than Ho in all sampled populations. Hardy-Weinberg equilibrium was found for some loci in different species. This is the first report of microsatellites successfully amplified in the whole Centaurium genus. They will be valuable for estimating mating system parameters and genetic diversity and exploring their relationships with the wide variation in flower morphology in the genus, especially anther-stigma separation.

Strong gene flow explains lack of mating system variation in the perennial herb, Vincetoxicum hirundinaria, in a fragmented landscape

Fragmented landscapes may have implications for the genetic structure of populations and for the microevolution of plant species. In particular, landscape fragmentation and/or population isolation might affect the evolution of plant mating systems. Here, we study the consequences of landscape fragmentation on the genetic structure of populations of a perennial herb, Vincetoxicum hirundinaria with a mixed mating system. Our study area, the south‐western Finnish archipelago, was formed after the glacial ice sheet started to retreat 12 000 years ago. Due to the isostatic land uplift following the glacial retreat, suitable habitats have been formed gradually, and as a consequence, populations of V. hirundinaria differ in age, size and their degree of isolation in the area. We hypothesized that a mixed‐mating system has been selected for in these populations due to the advantage of self‐fertilization in newly colonized areas and the advantage of outcrossing in adaptation to heterogeneous environments. To test this hypothesis, we collected seeds of open‐pollinated flowers from 13 V. hirundinaria populations differing in size, age and isolation, and used 15 microsatellite markers to perform progeny‐array analysis to estimate population‐level outcrossing rates, population genetic indices and population structure. We found that V. hirundinaria is almost completely outcrossing in the study area with no signs of past self‐fertilization and/or mating among relatives. The overall low inbreeding coefficients indicate that even in small populations mating among relatives is rare. High allelic richness of both maternal and offspring genotypes as well as limited genetic differentiation among the studied populations indicate strong gene flow among them. Our findings suggest that V. hirundinaria has successful seed and pollen dispersal among populations that has allowed colonization of new habitats in this fragmented landscape and led to a genetically well‐mixed group of populations at the scale of the study.

Self-compatibility and autonomous selfing of plants in meadow communities.

One of the most fundamental, although controversial, questions related to the evolution of plant mating systems is the distribution of outcrossing rates. Self-compatibility, and especially autonomous self-pollination, can become particularly beneficial in anthropogenically degraded habitats with impoverished pollinator assemblages and increased pollen limitation. In a hand-pollination experiment with 46 meadow plants from the Železné hory Mts., Czech Republic, we evaluated the species' ability to adopt different mating systems. For a subset of the species, we also tested seed germination for inbreeding depression. Subsequently, we analysed relationships between the species' mating systems and 12 floral and life-history traits. We found a relatively discrete distribution of the studied species into four groups. Fully and partially self-incompatible species formed the largest group, followed by self-compatible non-selfers and mixed mating species. The germination experiment showed an absence of inbreeding depression in 19 out of 22 examined species. Nectar sugar per flower, nectar sugar per shoot and dichogamy were significant associated with the mating system. Spontaneous selfing ability and self-incompatibility in species of the meadow communities had a discrete distribution, conforming to the general distribution of mating and breeding systems in angiosperms. The low frequency of spontaneous selfers and the lack of inbreeding depression at germination suggest the existence of a selection against selfing at the later ontogenetic stages. Some floral traits, such as the level of dichogamy and amount of nectar reward, may strongly impact the balance between selfing and outcrossing rates in the self-compatible species and thus shape the evolution of mating systems.

Does the evolution of self-fertilization rescue populations or increase the risk of extinction?

As a major evolutionary transition in seed plants, the evolution of plant mating systems has been much debated in evolutionary ecology. Over the last 10 years, well-established patterns of evolution have emerged. On the one hand, experimental studies have shown that self-fertilization is likely to evolve in a few generations (microevolution) as a response to rapid environmental change (e.g. pollinator decline), eventually rescuing a population. On the other, phylogenetic studies have demonstrated that repeated evolution towards self-fertilization (macroevolution) leads to a higher risk of lineage extinction and is thus likely to be disadvantageous in the long term. In either case - the short-term or long-term evolution of self-fertilization (selfing) - these findings indicate that a mating system is not neutral with respect to population or lineage persistence. They also suggest that selfing can have contrasting effects depending on time scale. This raises the question of whether mating system evolution can rescue populations facing environmental change. In this review, empirical and theoretical evidence of the direct and indirect effects of mating systems on population demography and lineage persistence were analysed. A simple theoretical evolutionary rescue model was also developed to investigate the potential for evolutionary rescue through selfing. Demographic studies consistently show a short-term advantage of selfing provided by reproductive assurance, but a long-term disadvantage for selfing lineages, suggesting indirect genomic consequences of selfing (e.g. mutation load and lower adaptability). However, our theoretical evolutionary rescue model found that even in the short term, while mating system evolution can lead to evolutionary rescue, it can also lead to evolutionary suicide, due to the inherent frequency-dependent selection of mating system traits. These findings point to the importance of analysing the demographic consequences of self-fertilization in order to predict the effect of selfing on population persistence as well as take into account the indirect genomic consequences of selfing. The pace at which processes such as inbreeding depression, purging, reproductive assurance and genomic rearrangements occur after the selfing transition is the key to clarifying whether or not selfing will result in evolutionary rescue.

Aggregate enantiostyly: Floral visitor interactions with a previously unreported form of floral display

Floral herkogamy, or the spatial separation of reproductive structures, plays an important role in the evolution of plant mating systems. One form of herkogamy is enantiostyly, or the alternate presentation of stigmas to the left and right of the floral axis. Theoretically, enantiostyly increases outcrossing rate by promoting reciprocal pollen deposition and export, but empirical evidence of this is lacking. Understanding how pollinators interact with enantiostylous flowers will illuminate the mechanisms by which enantiostyly encourages outcross pollination. We quantified style deployment within and among plants, of Allionia incarnata L. (Nyctaginaceae), a species with a new kind of enantiostyly we call “aggregate enantiostyly”. A. incarnata is the first species known to have “compound blossoms”, with different flowers each containing a left- or right-handed style. We quantify the autonomous selfing rate and describe floral visitor interactions with this unique floral structure. We found equal frequency of left- and right-handed blossoms within and among plants. Common floral visitors, Hemiargus ceraunus and Halictus sp., interacted with either anthers or stigmas, but not both, indicating effective outcrossing at the flower level. Outcrossing produced more fruits than selfing. The order in which floral visitors interacted with reproductive structures indicates that enantiostyly may increase pollen export. However, we did not find evidence that enantiostyly affected pollen deposition. Our study provides an intriguing first look at the reproductive ecology of a species with a new unique form of herkogamy, and provides evidence on the adaptive significance of enantiostyly.

Research Article Isolation and cross-amplification of fifteen microsatellites for oil-rewarding Calceolaria species (Calceolariaceae)

Calceolaria is a diversified American genus whose species are mainly visited by oil-collecting bees, representing a highly specialized plant-pollinator system. However, although this is a unique plant system, different aspects of its ecology and evolution remain unexplored. In this study we characterized fifteen polymorphic microsatellites for four Andean Calceolaria species using next-generation sequencing. The number of alleles per locus (Na) for the study species ranged from 2 to 11, and the observed (Ho) and expected (He) heterozygosity ranged from 0 to 0.85 and 0.3 to 0.87, respectively, while FIS ranged from 0.03 to 1.0. Among the four species, C. cana showed the greatest genetic diversity, followed by C. filicaulis. C. arachnoidea and C. lanigera showed similar, lower genetic diversity. These makers are a useful tool to conduct futures studies on population structure and gene flow. Specifically, this set of markers will be helpful to estimate selfing rates as a first approximation to the understanding of the role of specialization in plant mating system evolution

Inbreeding depression under mixed outcrossing, self-fertilization and sib-mating.

BackgroundBiparental inbreeding, mating between two relatives, occurs at a low frequency in many natural plant populations, which also often have substantial rates of self-fertilization. Although biparental inbreeding is likely to influence the dynamics of inbreeding depression and the evolution of selfing rates, it has received limited theoretical attention in comparison to selfing. The only previous model suggested that biparental inbreeding can favour the maintenance of stable intermediate selfing rates, but made unrealistic assumptions about the genetic basis of inbreeding depression. Here we extend a genetic model of inbreeding depression, describing nearly recessive lethal mutations at a very large number of loci, to incorporate sib-mating. We also include a constant component of inbreeding depression modelling the effects of mildly deleterious, nearly additive alleles. We analyze how observed rates of sib-mating influence the mean number of heterozygous lethals alleles and inbreeding depression in a population reproducing by a mixture of self-fertilization, sib-mating and outcrossing. We finally use the ensuing relationship between equilibrium inbreeding depression and population selfing rate to infer the evolutionarily stable selfing rates expected under such a mixed mating system.ResultsWe show that for a given rate of inbreeding, sib-mating is more efficient at purging inbreeding depression than selfing, because homozygosity of lethals increases more gradually through sib-mating than through selfing. Because sib-mating promotes the purging of inbreeding depression and the evolution of selfing, our genetic model of inbreeding depression also predicts that sib-mating is unlikely to maintain stable intermediate selfing rates.ConclusionsOur results imply that even low rates of sib-mating affect plant mating system evolution, by facilitating the evolution of selfing via more efficient purging of inbreeding depression. Alternative mechanisms, such as pollination ecology, are necessary to explain stable mixed selfing and outcrossing.

Pollinator specialization: from the individual to the community.

1190 I. 1190 II. 1191 III. 1191 IV. 1193 V. 1193 1194 References 1194 SUMMARY: Most spermatophytes need conspecific pollen in order to produce seed. This need for specialization seems to conflict with the generalized nature of most plant-pollinator interactions. Specialization and generalization are dynamic - not fixed - and exist simultaneously in multiple states at different levels of biological hierarchy. Over the short term, specialization ensures conspecific pollen transfer, whereas over the long term, generalization improves system-level robustness. The balance between specialization and generalization at different scales is critical for different kinds of ecological functioning and is an important factor in plant speciation and the evolution of plant mating systems. Community context, including diversity and interaction network structure at different levels of aggregation, is a key driver of specialization dynamics.

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Previous articleNext article FreeAnnouncementEditor-in-Chief: Judith L. BronsteinEditor-in-Chief: Judith L. Bronstein Search for more articles by this author PDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinked InRedditEmailQR Code SectionsMoreDr. Alice Winn of Florida State University began a three-year term as editor of The American Naturalist in July 2015, replacing Susan Kalisz, who wrapped up a highly successful tenure on the Editorial Board this summer. Dr. Winn is an exceptionally talented evolutionary biologist and ecologist. She received her BSc in biology from Bates College in 1979 and her PhD from Michigan State University in 1984. She carried out postdoctoral research at Ohio State University and the University of Chicago and has been a member of the faculty in the Department of Biological Science at Florida State University since 1990. The central theme of research in her lab is adaptation to variable environments, with particular focus on local adaptation, the ecology and evolution of phenotypic plasticity, and plant mating system evolution. She is an experienced editor and reviewer and currently is Associate Chair for Academic Programs in her department. She plays a pivotal role on The American Naturalist’s Editorial Board, bridging plant ecology, evolutionary theory, and genetics. We welcome Dr. Winn and look forward to working with her. Previous articleNext article DetailsFiguresReferencesCited by The American Naturalist Volume 187, Number 1January 2016 Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/684189 Views: 327Total views on this site © 2015 by The University of Chicago. All rights reserved.PDF download Crossref reports no articles citing this article.

Constraints imposed by pollinator behaviour on the ecology and evolution of plant mating systems.

Most flowering plants rely on pollinators for their reproduction. Plant-pollinator interactions, although mutualistic, involve an inherent conflict of interest between both partners and may constrain plant mating systems at multiple levels: the immediate ecological plant selfing rates, their distribution in and contribution to pollination networks, and their evolution. Here, we review experimental evidence that pollinator behaviour influences plant selfing rates in pairs of interacting species, and that plants can modify pollinator behaviour through plastic and evolutionary changes in floral traits. We also examine how theoretical studies include pollinators, implicitly or explicitly, to investigate the role of their foraging behaviour in plant mating system evolution. In doing so, we call for more evolutionary models combining ecological and genetic factors, and additional experimental data, particularly to describe pollinator foraging behaviour. Finally, we show that recent developments in ecological network theory help clarify the impact of community-level interactions on plant selfing rates and their evolution and suggest new research avenues to expand the study of mating systems of animal-pollinated plant species to the level of the plant-pollinator networks.

Phenotypic plasticity in mating-system traits in the annual Collinsia verna

Variation in abiotic factors can influence the selective advantage of selfing and expression of the mating system if mating-system modifier traits are phenotypically plastic. However, relative to biotic factors, the role of abiotic conditions in driving variation in and evolution of plant mating systems is rarely addressed. We use an experimental approach to evaluate the extent to which genetic and environmental variation influence the expression of mating-system traits in the annual Collinsia verna. We subjected families to two environmental treatments in the greenhouse that varied in light and water availability, simulating natural and short flowering-season conditions, and examined the following: autonomous fruit set, flower number, flower size, rate of anther dehiscence, floral longevity, and timing of selfing. Our results demonstrate plasticity in nearly all traits examined. Compared with natural-season conditions, plants under short-season conditions produced fewer, smaller flowers and selfed approximately one day later due to slower anther dehiscence rates. Autonomous fruit set was similar across treatments, but there was genetic variation for plasticity in this important trait. Further, we show genetic variation in autonomous fruit set, timing of selfing, and flower number and size. Given the effects of global climate change on the duration of growing season, our results suggest that plasticity in mating-system traits will affect mating-system variation and, thus, opportunities for selection.

EVALUATING A SIMPLE APPROXIMATION TO MODELING THE JOINT EVOLUTION OF SELF-FERTILIZATION AND INBREEDING DEPRESSION

A comprehensive understanding of plant mating system evolution requires detailed genetic models for both the mating system and inbreeding depression, which are often intractable. A simple approximation assuming that the mating system evolves by small infrequent mutational steps has been proposed. We examine its accuracy by comparing the evolutionarily stable selfing rates it predicts to those obtained from an explicit genetic model of the selfing rate, when inbreeding depression is caused by partly recessive deleterious mutations at many loci. Both models also include pollen limitation and pollen discounting. The approximation produces reasonably accurate predictions with a low or moderate genomic mutation rate to deleterious alleles, on the order of U = 0.02-0.2. However, for high mutation rates, the predictions of the full genetic model differ substantially from those of the approximation, especially with nearly recessive lethal alleles. This occurs because when a modifier allele affecting the selfing rate is rare, homozygous modifiers are produced mainly by selfing, which enhances the opportunity for purging nearly recessive lethals and increases the marginal fitness of the allele modifying the selfing rate. Our results confirm that explicit genetic models of selfing rate and inbreeding depression are required to understand mating system evolution.

Following Darwin's trail: Interactions affecting the evolution of plant mating systems

• 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.

FUNCTIONAL PLEIOTROPY AND MATING SYSTEM EVOLUTION IN PLANTS: FREQUENCY-INDEPENDENT MATING

Mutations that alter the morphology of floral displays (e.g., flower size) or plant development can change multiple functions simultaneously, such as pollen export and selfing rate. Given the effect of these various traits on fitness, pleiotropy may alter the evolution of both mating systems and floral displays, two characters with high diversity among angiosperms. The influence of viability selection on mating system evolution has not been studied theoretically. We model plant mating system evolution when a single locus simultaneously affects the selfing rate, pollen export, and viability. We assume frequency-independent mating, so our model characterizes prior selfing. Pleiotropy between increased viability and selfing rate reduces opportunities for the evolution of pure outcrossing, can favor complete selfing despite high inbreeding depression, and notably, can cause the evolution of mixed mating despite very high inbreeding depression. These results highlight the importance of pleiotropy for mating system evolution and suggest that selection by nonpollinating agents may help explain mixed mating, particularly in species with very high inbreeding depression.

New perspectives on the evolution of 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 Viewpoint paper 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. This Viewpoint also serves as the introduction to a Special Issue on the Evolution of Plant Mating Systems. The 15 papers in this special issue provide inspiring examples of recent discoveries, and glimpses of exciting developments yet to come.

RAPID EVOLUTION CAUSED BY POLLINATOR LOSS IN MIMULUS GUTTATUS

Anthropogenic perturbations including habitat loss and emerging disease are changing pollinator communities and generating novel selection pressures on plant populations. Disruption of plant-pollinator relationships is predicted to cause plant mating system evolution, although this process has not been directly observed. This study demonstrates the immediate evolutionary effects of pollinator loss within experimental populations of a predominately outcrossing wildflower. Initially equivalent populations evolved for five generations within two pollination treatments: abundant bumblebee pollinators versus no pollinators. The populations without pollinators suffered greatly reduced fitness in early generations but rebounded as they evolved an improved ability to self-fertilize. All populations diverged in floral, developmental, and life-history traits, but only a subset of characters showed clear association with pollination treatment. Pronounced treatment effects were noted for anther-stigma separation and autogamous seed set. Dramatic allele frequency changes at two chromosomal polymorphisms occurred in the no pollinator populations, explaining a large fraction of divergence in pollen viability. The pattern of phenotypic and genetic changes in this experiment favors a sequential model for the evolution of the multitrait "selfing syndrome" observed throughout angiosperms.

The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards

Summary1. The evolution of flowering plants has undoubtedly been influenced by a pollinator’s ability to learn to associate floral signals with food. Here, we address the question of ‘why’ flowers produce scent by examining the ways in which olfactory learning by insect pollinators could influence how floral scent emission evolves in plant populations.2. Being provided with a floral scent signal allows pollinators to learn to be specific in their foraging habits, which could, in turn, produce a selective advantage for plants if sexual reproduction is limited by the income of compatible gametes. Learning studies with honeybees predict that pollinator‐mediated selection for floral scent production should favour signals which are distinctive and exhibit low variation within species because these signals are learned faster. Social bees quickly learn to associate scent with the presence of nectar, and their ability to do this is generally faster and more reliable than their ability to learn visual cues.3. Pollinators rely on floral scent as a means of distinguishing honestly signalling flowers from deceptive ones. Furthermore, a pollinator’s sensitivity to differences in nectar rewards can bias the way that it responds to floral scent. This mechanism may select for flowers that provide olfactory signals as an honest indicator of the presence of nectar or which select against the production of a detectable scent signal when no nectar is present.4. We expect that an important yet commonly overlooked function of floral scent is an improvement in short‐term pollinator specificity which provides an advantage to both pollinator and plant over the use of a visual signal alone. This, in turn, impacts the evolution of plant mating systems via its influence on the species‐specific patterns of floral visitation by pollinators.

Evolution towards self‐compatibility when mates are limited

Theory of plant mating system evolution predicts the spread of self-compatibility (SC) in a predominantly self-incompatible population when inbreeding depression (ID; the decline in fitness because of selfing) is small and when compatible mates are limited. I tested these two predictions by measuring the occurrence of SC in 13 natural populations of Ranunculus reptans L. that varied in ID and frequency of cross-incompatible mates. Enforced selfing experiments were conducted in 2 years. In the first year, self-pollination was applied at two flower ages to investigate the occurrence of delayed SC. I found that SC was not uncommon across all populations, but self-compatible plants usually produced few seeds. There was no evidence for delayed SC. The occurrence of SC was not associated with population-level ID, but populations with more limited availability of compatible mates had a significantly higher frequency of plants that were at least partially self-compatible. The results indicate that, in R. reptans, a shortage of available mates in small populations may cause the evolution of partial SC and mixed mating.