The Mating Flower


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Goodwillie, C. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Harder, L. Ecology and Evolution of Flowers. Oxford: Oxford University Press. Harding, J. Genetics of Lupinus. Genetic variability, heterozygosity and outcrossing in colonial populations of Lupinus succulentus. Evolution 31, — PubMed Abstract Google Scholar. Herlihy, C.


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Genetic cost of reproductive assurance in a self-fertilizing plant. Nature , — Igic, B. The distribution of plant mating systems: study bias against obligately outcrossing species. Ivey, C. Tests for the joint evolution of mating system and drought escape in Mimulus.

Jarne, P. Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Johnston, M. Correlations among fertility components can maintain mixed mating in plants. Kalisz, S. Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed-mating genus Collinsia. Kalyaanamoorthy, S. ModelFinder: fast model selection for accurate phylogenetic estimates.

Methods Kameyama, Y. Flowering phenology influences seed production and outcrossing rate in populations of an alpine snowbed shrub, Phyllodoce aleutica : effects of pollinators and self-incompatibility. Karron, J. New perspectives on the evolution of plant mating systems. Outcrossing rates of individual Mimulus ringens genets are correlated with anther-stigma separation. Heredity 79, — Effects of floral display size on male and female reproductive success in Mimulus ringens. The influence of population density on outcrossing rates in Mimulus ringens.

Heredity 75, — Kearse, M. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, — Keck, F. Kelly, J. A manipulative experiment to estimate biparental inbreeding in monkeyflowers.

Plant Sci. Knight, T. Pollen limitation of plant reproduction: pattern and process. Kruszewski, L. Explaining outcrossing rate in Campanulastrum americanum Campanulaceae : geitonogamy and cryptic self-incompatibility. Kubota, S. Adaptive significance of self-fertilization in a hermaphroditic perennial, Trillium camschatcense Melanthiaceae. Lande, R. The evolution of self-fertilization and inbreeding depression in plants. Genetic models. Evolution 39, 24— Lanfear, R. Estimating phylogenies for species assemblages: a complete phylogeny for the past and present native birds of New Zealand. Lloyd, D.

Self-and cross-fertilization in plants. The selection of self-fertilization. Google Scholar. Functional dimensions. Mitchell, R. New frontiers in competition for pollination. The influence of Mimulus ringens floral display size on pollinator visitation patterns. Moeller, D. Global biogeography of mating system variation in seed plants. Ecological context of the evolution of self-pollination in Clarkia xantlana : population size, plant communities, and reproductive assurance. Evolution 59, — Molina-Freamer, F. Breeding systems of hermaphroditic and gynodioecious populations of the colonizing species Trifolium hirtum all in California.

Morgan, M. Plant population dynamics, pollinator foraging, and the selection of self-fertilization. How to measure and test phylogenetic signal. Methods Ecol. Murawski, D. The effect of the density of flowering individuals on the mating systems of nine tropical tree species. Heredity 67, — Nguyen, L.

Nora, S. High Correlated paternity leads to negative effects on progeny performance in two mediterranean shrub species. Peter, C. A pollinator shift explains floral divergence in an orchid species complex in South Africa. Porcher, E. The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. Raijmann, L. Genetic variation and outcrossing rate in relation to population size in Gentiana pneumonanthe L.

Ritland, K. The genetic mating structure of subdivided populations I. Open-mating model. Inferences about inbreeding depression based on changes of the inbreeding coefficient. Extensions of models for the estimation of mating systems using n independent loci. Heredity 88, — A model for the estimation of outcrossing rate and gene frequencies using n independent loci.

Heredity 47, 35— Routley, M. Effect of population size on the mating system in a self-compatible, autogamous plant, Aquilegia canadensis Ranunculaceae. Heredity 82, — Schemske, D. Empirical observations. Evolution 39, 41— Sorin, Y. Effects of pollination and postpollination processes on selfing rate in Mimulus ringens. Spigler, R. Increased inbreeding but not homozygosity in small populations of Sabatia angularis Gentianaceae.

Plant Syst. Stebbins, G. Self fertilization and population variability in the higher plants. Sun, M. Floral adaptation to local pollinator guilds in a terrestrial orchid. Tedder, A. Sporophytic self-incompatibility genes and mating system variation in Arabis alpina. Tummers, B. DataThief III. Vogler, D. Sex among the flowers: the distribution of plant mating systems. Evolution 55, — Waycott, M. The mating system of an hydrophilous angiosperm Posidonia australis Posidoniaceae.

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After signing up, we'll send an email with a link to click to confirm your subscription. It's our way of making sure we're not accidentally sending you spam. Saturday, July 6, Botany One. Reductions in herkogamy with flower positions may be expected in environments with either low pollinator abundance or low nutrients. The model consists of a sympodial succession of equivalent sympodial units metamers , each of which is orthotropic and determinate in its growth. For example, Goodwillie et al.

The wide mating system surveys reported in Goodwillie et al. However, an important limitation of this approach is that most published outcrossing rates report data sampled from just one or two populations Goodwillie et al. As noted by Schemske and Lande , a species-level mean cannot adequately characterize highly variable species. Similarly, representing species outcrossing rates by only one or two population estimates potentially overlooks substantial and important variation in outcrossing rate within species.

We lack quantitative estimates of the prevalence and magnitude of among-population variation in outcrossing rates, despite discussion in the early literature Schemske and Lande, ; Barrett and Eckert, This broad view is important, because if variation among populations is typically small, then estimates from one or two populations will adequately characterize the mating system of a species.

Alternatively, substantial variation among populations provides crucial information needed to explore the evolution of mating-system diversity, and compels researchers to routinely assess multiple populations in mating system studies. Obtaining a wider view on the distribution of among-population variation in outcrossing rates will also be useful for addressing questions concerning the evolution of such variation. For example, do closely related species tend to have more similar among-population variation than expected by chance? The extent to which mating system variance correlates with phylogenetic distance could help to ascertain the relative influence of environmental vs.

Among-population variation in mating system might also be linked to specific ecological influences. For example, biotically-pollinated species more commonly have mixed mating systems, relative to wind-pollinated species Schemske and Lande, ; Aide, ; Barrett and Eckert, It has been suggested that the consistency of abiotic factors wind pollination is greater than that of biotic-pollination, as the availability of animal pollinators can vary widely between sites and seasons.

Theoretically, this should drive higher variance in outcrossing rate among populations of biotically-pollinated plants Aide, ; Barrett and Eckert, ; Waycott and Sampson, , yet this hypothesis has not previously been tested.


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  • Early work on outcrossing rates was largely based on imprecise estimates from single-gene morphological polymorphisms Harding and Barnes, ; Schemske and Lande, , whereas today the availability of molecular markers coupled with maximum likelihood multilocus outcrossing measures Ritland, yield more precise estimates of population outcrossing rates.

    Over the last decade the number of studies reporting molecular marker-based outcrossing rates from three or more populations has nearly doubled, facilitating a detailed, population-level perspective on the distribution of outcrossing rate variation. We therefore surveyed more than 30 years of plant mating system studies in the literature, focusing on those studies presenting multi-population estimates of outcrossing. With these data, we then ask whether variance in the mating system is correlated to phylogeny or pollination mode and discuss the extent of among-population variation in plant mating systems.

    To measure variability in population-level estimates of outcrossing rate we assembled a database of studies reporting outcrossing rates t m for three or more populations per species. We focused exclusively on multilocus estimates of outcrossing rate because these estimates best distinguish true selfing from biparental inbreeding Ritland, , and are less influenced by selection than are single locus estimates Ritland, The maximum likelihood multilocus outcrossing measure t m Ritland and Jain, incorporated in software programs MLT Ritland, b and MLTR Ritland, is the most widely used estimator of the outcrossing rate.

    We therefore searched for all studies reported in Web of Science through Sept 1, that cited one of the two software programs Ritland, b , or the paper first formalizing t m Ritland and Jain, From this set of papers, we extracted a dataset of population-level multilocus outcrossing estimates t m for flowering plants. To capture variation among populations our inclusion criteria required each study to have sampled a minimum of three populations for any one species or subspecies. We excluded population t m estimates derived from experimentally manipulated populations, planted crops, and seed orchards.

    Selfing in hermaphrodite angiosperms can occur within flowers either autogamously or facilitated by pollen vectors. Within-flower selfing does not occur in gymnosperms, and we therefore excluded them from our analysis in order to unite our dataset under a common paradigm of selfing. Similarly, we also excluded data from male-sterile plants in gynodioecious angiosperms.

    We collected the reported standard error s. We set an inclusion threshold for s. We also collected information on the pollination mode for each species by referring to the papers reporting t m , or when not reported, referring elsewhere in the primary literature. Ten studies reported data for the same population over multiple years and in those cases we used the mean population t m across years. In a few cases, separate papers reported the same data for one or more populations, and we therefore used the supplied population codes to exclude duplicate populations.

    In 13 studies reporting separate t m for different flower or seed morphs within a population we calculated the mean t m for each population across those categories. Where t m or s. We performed an analysis testing for phylogenetic signal in both mean and variance of t m. For this, we generated a phylogeny for the species in our dataset using matK accessions obtained from NCBI Genbank, using sequences from the genus when sequences from the species were not available following Lanfear and Bromham, We used Modelfinder Kalyaanamoorthy et al.

    Significance in Moran's I was assessed through bootstrap permutations. We tested for a difference in variance of t m between biotic and abiotically pollinated species using an analysis that accounted for the fact that a 0—1 bounded estimate such as t m will naturally exhibit lower variance at the extreme values. This ratio estimates how well the observed variance matches expected binomial variance under the average t m and when treated as a response variable avoids the influence of intermediate values of t m inflating variance. Our dataset includes t m and s. The number of population t m estimates per species ranged from 3 to 37, the mean was 7.

    In total, studies met our inclusion criteria, with the number of studies approximately doubling each decade.

    Many species in our survey exhibited substantial among-population variation in outcrossing rate Figure 1. In the six most variable species, the s. Species with the highest among-population variation in t m include: T. As expected for a 0—1 bounded variable, among-population variation in t m estimates was lowest for species with extremely high or extremely low mean outcrossing rates Figure S2.

    The among-population s. Figure 1. Population-level outcrossing rates t m for plant species, arranged in order of decreasing species mean t m. The distribution of t m estimates in our dataset appears similar to the distribution of species means for species reported by Goodwillie et al. While Goodwillie et al. Only one species T. Four taxa were not included in the matK phylogeny, as they did not have Genbank accessions Banksia sphaerocarpa, Banksia oligantha , and Tetratheca paynterae , and one species Tolpis laciniata was removed due to its inexplicable placement on an extremely long branch.

    While the highest values of among-population variance were found in biotically pollinated species Figure 2 , the difference in variance between pollination modes was not significant according to our bootstrapped test of binomial variance 0. Figure 2. Variance in t m among populations in 87 species of biotically-pollinated and 10 species of abiotically-pollinated flowering plants. Lower and upper hinges correspond to 25 and 75th percentiles, internal horizontal bars indicate the median, vertical whiskers extends up to the largest value and down to the lowest values no further than 1.

    Points outlying this are represented as dots. Our review of population-level outcrossing reveals prevalent and substantial among-population variation in the mating system of many flowering plant species. As for previous work, the high frequency of mixed mating is difficult to reconcile with classical models that predict a bimodal distribution of t m Lande and Schemske, ; Charlesworth et al. It is difficult to find evidence in our study to support the hypothesis that biotic pollination drives mating system variance, relative to abiotic pollination Schemske and Lande, ; Aide, ; Barrett and Eckert, Although visual inspection of Figure 2 shows many more points with large variation for biotically pollinated species, our statistical analysis suggests that this is an illusion resulting from the necessary relationship between mean and variance for traits constrained to values between 0 and 1.

    Since many of the abiotically pollinated species had very low or very high outcrossing rates, they necessarily had low variance among populations. In our analysis, we attempted to control for this, and the lack of significant difference leads us to conclude that wind pollinated species are restricted in their variance because of more common obligate selfing or outcrossing, rather than because of any association with the pollen vector itself.

    This leads to the question of why wind pollinated species might more frequently evolve obligate selfing or outcrossing, which may hinge on important differences in pollen transport dynamics under biotic vs. Our phylogenetic comparative analysis found no support in Moran's I for a correlation of among population variance in outcrossing rates with phylogeny. This implies that mating system variance might be evolving too fast, or too slow, to be reflected by phylogeny.

    Additionally, a strong intervening influence of environmental or ecological drivers of t m variance might be sufficient to obscure signal in traits that might actually be correlated to phylogeny. Weak but significant phylogenetic correlation in mean t m supports the previous findings of Moeller et al. Among-population variation in outcrossing rate may reflect the influence of ecological factors that affect the proportion of self pollen deposited on stigmas Karron et al.

    It is important to distinguish these two broad causes of among-population variation because they differ in their predicted effects on the evolution of mating systems. Ecological factors exert important short-term effects that can create mating system variance, but by virtue of their stochasticity they will vary in the strength of their influence on adaptation. In contrast, heritable mating system traits dictate long term evolutionary behavior of the mating system Devaux et al.

    The complex interaction of environmental and heritable mating system traits ultimately directs adaptation in the mating system; for example, pollinator availability strongly influences the fitness benefits of heritable floral traits that promote outcrossing Eckert et al. The wide range of potential drivers of mating system variance is reflected by studies of the most variable species in our database.

    Ecological factors influencing the quantity and quality of pollen delivery include pollinator abundance Knight et al. Many of these ecological factors vary temporally as well as spatially, leading to within-year or among-year variation in outcrossing rate Brunet and Sweet, ; Eckert et al. Ecological factors can, therefore, cause dynamic shifts in mating system over short periods, potentially making single season observations difficult to interpret, and violating assumptions of analyses assuming constant t m Ritland, a ; Routley et al.

    Few studies have quantified outcrossing rates of populations over multiple years, and a smaller subset have linked this variation to changes in ecological factors among years Eckert et al. Our survey included 10 studies with multi-year outcrossing estimates for the same populations, however most of those did not include more than two time-point estimates for more than three populations. While a statistical analysis of among-year, vs. Genetic factors also influence the mating system. Key among these is the magnitude of inbreeding depression Porcher and Lande, ; Devaux et al.

    Sex among the flowers: the distribution of plant mating systems.

    Among-population variation in outcrossing rates may also reflect the influence of heritable traits that vary within and among populations, such as floral morphology and floral display Epperson and Clegg, ; Lloyd and Schoen, ; Harder and Barrett, ; Eckert et al. Adding further complexity, some traits that influence the mating system, such as flower size, can be under interacting genetic and environmental control Elle and Hare, ; Ivey and Carr, , making it difficult to unambiguously identify the genetic component of variation in mating system see below. In light of prevalent among-population variation in plant mating systems, future studies should characterize the outcrossing rate of several populations of each species, and should treat the mean outcrossing rate of each species with caution.

    The most informative studies will also report ecological and genetic axes of variation that correlate with mating system variation. Since ecological drivers of outcrossing rates may vary temporally Brunet and Sweet, ; Eckert et al. Indeed, one hypothesis for the evolution of selfing suggests that high temporal variance in pollinator service might select for selfing as a means of reproductive assurance Stebbins, ; Barrett and Husband, a ; Cheptou, ; Morgan et al. This needs to be tested with a longitudinal design that explicitly measures variance in pollinator community and visitation alongside measures of outcrossing over multiple seasons.

    Frontiers | Plant Mating Systems Often Vary Widely Among Populations | Ecology and Evolution

    One challenge when linking ecological factors with mating system variation is that multiple ecological variables are commonly confounded Barrett and Eckert, For example, floral display size may correlate with population density Karron et al. Confounding factors are best addressed through factorial experimental designs, where populations represent different combinations of the variables under study. For example, translocation experiments can address how the local pollination environment influences among-population variation in outcrossing rate.

    Although translocation studies have rarely been used in mating system research cf. Kelly and Willis, , they have been effective in studies of adaptive divergence in floral morphology ecotypes associated with differences in pollinator community Peter and Johnson, ; Sun et al. In mating system work, individuals could be translocated from a focal population into a different pollination environment. Any associated differences in mating system between translocated and non-translocated plants indicates an environmental influence on the mating system.

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    Manipulative studies also provide the opportunity to explore how genetic factors influence the mating system. Common garden experiments, for example, are an underused but powerful way to control for the influence of environmental variation. By subjecting plants from several source populations to a common pollination context, and controlling environmental variation that may influence plastic traits such as flower size, these experiments are ideal for understanding the influence of genotype on the mating system Elle and Hare, ; Karron and Mitchell, Although seldom assessed, outcrossing rate variation among individuals may be nearly as large as variation among populations Karron et al.

    This variation in outcrossing rate among individuals is also open to study by many of the correlative and experimental approaches described above. Floral traits, density, phenology, and co-flowering community can all vary on a fine sub-population scale, and the influence of these factors on the emergent mating system could productively be assessed by studies at the sub-population level.

    There are several characteristics of our database that may influence the distribution of reported outcrossing rates.

    References

    Our finding of no correlation in t m variance with phylogeny provides evidence that our data are not unduly influenced by these over-represented families. Second, our sample only includes studies reporting t m for three or more populations. If researchers are biased against making replicate outcrossing measures across populations when they do not expect to find variation, our results might also be biased toward over-representing species with t m variance. Third, when sampling a species, instead of sampling populations randomly, researchers may bias their sample to populations they expect will display wide variation in outcrossing Schemske and Lande, If this were occurring, our measures of species' variance in t m would be over-estimated relative to the true variance.

    Lastly, the proportion of mixed-mating species in our sample may be overestimated because researchers focusing on self-incompatible species may be less likely to measure among-population variation in outcrossing rates creating a bias against the appearance of obligate outcrossers in our dataset Igic and Kohn, Prevalent and substantial among-population variation in outcrossing rates highlights the need for caution in both estimation and interpretation of outcrossing rates in flowering plants.

    Estimates from single populations should not be used to characterize the mating system of an entire species.

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