Pollination of two species of Vellozia (Velloziaceae) from high-altitude quartzitic grasslands, Brazil
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The pollinators and breeding system of two species of Vellozia (Velloziaceae) from high-altitude quartzitic grasslands in SE Brazil were studied. Vellozia leptopetala is shrubby and grows solely on rocky outcrops, V. epidendroides is herbaceous and grows on stony soils. Both bear solitary, hermaphrodite flowers, and have massive, short-lasting annual blooms. We evaluated the level of self-compatibility and need for pollinators of 50 plants of each species and 20-60 flowers per treatment: hand self- and cross-pollination, spontaneous pollination, agamospermy and control. The behavior of floral visitors on flowers and within plants was recorded. Both species are mostly self-incompatible, but produce a small number of seeds by self-fertilization. The pollen-ovule ratio suggests facultative xenogamy. They were visited primarily by bees, of which the most important pollinators were two leaf-cutting bees (Megachile spp.). Vellozia leptopetala was also pollinated by a territorial hummingbird. Low natural seed production compared to cross-pollination seed numbers suggests that pollen limitation is the main cause of low seed set. This was attributed to the combined effect of five mechanisms: selfing prior to anthesis, enhanced geitonogamy as a result of large floral displays, low number of visits per flower for the same reason, pollen theft by many insect species, and, in V. leptopetala, delivery of mixed pollen loads on the stigma as a consequence of hummingbird promiscuity.Keywords:
Hummingbird
Selfing
Outcrossing
Orchidaceae
Premise of research. Pollinators are known to impose strong selection on floral shape. Particularly well studied is the relationship between the flowers of hummingbird-pollinated plant species and the bills of their pollinators. However, no studies to date have evaluated whether these relationships vary according to the level of pollination specialization. Here, we quantify the relationship between the corolla shape of Antillean Gesneriaceae and the bills of their hummingbird pollinators for species with a specialist (one functional group of pollinators: hummingbirds) and a generalist (more than one functional group of pollinators: hummingbirds, bats, and insects) pollination strategy.Methodology. We used phylogenetic generalized least squares analyses on linear measurements and phylogenetic two blocks partial least squares on multivariate geometric morphometrics data to test whether and how the variation in the corolla shape of the Antillean Gesneriaceae is correlated to the shape of the bills of their hummingbird pollinators.Pivotal results. We found that corolla shape is correlated with the bill shape of the hummingbird pollinators but that the nature of this relationship differed between pollination specialists and generalists. For example, corolla curvature was positively correlated with bill curvature for specialists but not for generalists.Conclusions. Our study suggests that pollinators affect the evolution of flower shape but that the nature and strength of the selective pressures are affected by the pollinator guild of the pollinators in the Antillean Gesneriaceae.
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Gesneriaceae
Zoophily
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Abstract The transition to self-compatibility from self-incompatibility is often associated with high rates of self-fertilization, which can restrict gene flow among populations and cause reproductive isolation of self-compatible (SC) lineages. Secondary contact between SC and self-incompatible (SI) lineages might re-establish gene flow if SC lineages remain capable of outcrossing. By contrast, intrinsic features of SC plants that reinforce high rates of self-fertilization could maintain evolutionary divergence between lineages. Arabidopsis lyrata subsp. lyrata is characterized by multiple origins of self-compatibility and high rates of self-fertilization in SC-dominated populations. It is unclear whether these high rates of selfing by SC plants have intrinsic or extrinsic causes. We estimated outcrossing rates and examined patterns of pollinator movement for 38 SC and 40 SI maternal parents sampled from an admixed array of 1509 plants sourced from six SC and six SI populations grown under uniform density. Although plants from SI populations had higher outcrossing rates (mean t m = 0.78 ± 0.05 SE) than plants from SC populations (mean t m = 0.56 ± 0.06 SE), outcrossing rates among SC plants were substantially higher than previous estimates from natural populations. Patterns of pollinator movement appeared to contribute to lower outcrossing rates for SC plants; we estimated that 40% of floral visits were geitonogamous (between flowers of the same plant). The relatively high rates of outcrossing for SC plants under standardized conditions indicate that selfing rates in natural SC populations of A. lyrata are facultative and driven by extrinsic features of A. lyrata , including patterns of pollinator movement.
Outcrossing
Selfing
Outbreeding depression
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A bimodal distribution of outcrossing rates was observed for natural plant populations, with more primarily selfing and primarily outcrossing species, and fewer species with intermediate outcrossing rate than expected by chance. We suggest that this distribution results from selection for the maintenance of outcrossing in historically large, outcrossing populations with substantial inbreeding depression, and from selection for selfing when increased inbreeding, due to pollinator failure or population bottlenecks, reduces the level of inbreeding depression. Few species or populations are fixed at complete selfing or complete outcrossing. A low level of selfing in primarily outcrossing species is unlikely to be selectively advantageous, but will not reduce inbreeding depression to the level where selfing is selectively favored, particularly if accompanied by reproductive compensation. Similarly, occasional outcrossing in primarily selfing species is unlikely to regularly provide sufficient heterosis to maintain selection for outcrossing through individual selection. Genetic, morphological and ecological constraints may limit the potential for outcrossing rates in selfers to be reduced below some minimum level.
Outcrossing
Selfing
Outbreeding depression
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Outcrossing
Selfing
Plant biochemistry
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The adaptive accuracy of flowers in the context of pollination can be used to address the relationships between flower phenotype (fundamental pollination accuracy and precision) and realized accuracy and precision (interaction of floral parts with a pollinator). Here we tested whether effectiveness (number of pollen grains transported per visit) and realized male and female accuracy and precision differ between two hummingbird pollinator species (Heliomaster furcifer and Sappho sparganura) that pollinate the ornithophilous liana Dolichandra cynanchoides. Although the hummingbird species did not differ in the frequency of flower visitation, H. furcifer carried pollen on a narrower spot of the head and deposited significantly more pollen on a restricted zone of artificial stigmas − representative of the true stigma − compared with S. sparganura. Flower structure exhibited similar accuracy with regard to pollen deposition on and retrieval from pollinators. Functional flower depth matched significantly with the bill of the hummingbird exhibiting the highest precision and accuracy. This suggests that mechanical reciprocal fit may be responsible for the better pollination performance of H. furcifer. In this study we show that differences in realized accuracy and precision may explain evolutionary responses to pollinator specialization in a single pollinator species within functional groups.
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The evolutionary transition from diploidy to polyploidy is prevalent in flowering plants and may result in correlated changes in mating system (outcrossing rate). Most theory predicts a shift toward self‐fertilization (decrease in outcrossing) in polyploids, but empirical evidence for this pattern and its underlying mechanisms is inconclusive or restricted to a few cases. In an analysis of variation in outcrossing rates among diploid‐polyploid species pairs from the literature, polyploids had lower outcrossing rates (higher selfing; $$t=0.23$$, $$\mathrm{SE}\,=0.09$$) than diploids ($$t=0.52$$, $$\mathrm{SE}\,=0.12$$). Among polyploids, however, allopolyploids were predominantly selfing ($$t=0.20$$, $$\mathrm{SE}\,=0.099$$), whereas autopolyploids had significantly higher outcrossing rates ($$t=0.64$$, $$\mathrm{SE}\,=0.087$$), raising the question of what limits the evolution of selfing in autopolyploids. To address this, we examined the magnitude of inbreeding depression in synthetic polyploids of the plant Chamerion angustifolium. The intrinsic cost of selfing in newly formed polyploids was negligible compared with extant polyploids, thus promoting the spread of selfing. However, there was weak evidence that inbreeding depression increases with history of inbreeding, suggesting that the rise in selfing may be ephemeral and that selection ultimately favors mixed or outcrossed mating systems in autopolyploids. Such constraints on selfing have some theoretical support, but additional research on patterns of variation and genetic mechanisms governing polyploid mating systems are needed.
Selfing
Outcrossing
Polyploid
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Classic deterministic genetic models of the evolution of selfing predict species should be either completely outcrossing or completely selfing. However, even species considered high selfers outcross to a small degree (e.g. Arabidopsis thaliana and Caenorhabditis elegans). This discrepancy between theory and data may exist because the classic models ignore the effects of drift interacting with selection, that is, Hill-Robertson effects. High selfing rates make the effective rate of recombination near zero, which is expected to cause the build-up of negative disequilibria in finite populations. Despite the transmission advantage associated with complete selfing, low levels of outcrossing may be favoured because of the benefits of increasing the effective rate of recombination to dissipate negative disequilibria. Using multilocus simulations, we confirm that selfing reduces effective population size through background selection and causes negative disequilibria between selected sites. Consequently, the rate of adaptation is substantially reduced in strong selfers. When selfing rate is allowed to evolve, populations evolve to be either strong outcrossers or strong selfers, depending on the parameter values. Amongst selfers, low, but nonzero, levels of outcrossing can be maintained by selection even when all mutations are deleterious; more outcrossing is maintained with higher rates of deleterious mutation. The addition of beneficial mutations can (i) lead to a quantitative increase in the degree of outcrossing amongst stronger selfers but (ii) may cause outcrossing species to evolve into stronger selfers.
Selfing
Outcrossing
Local adaptation
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Hermaphroditic plants can potentially self-fertilize, but most possess adaptations that promote outcrossing. However, evolutionary transitions to higher selfing rates are frequent. Selfing comes with a transmission advantage over outcrossing, but self-progeny may suffer from inbreeding depression, which forms the main barrier to the evolution of higher selfing rates. Here, we assessed inbreeding depression in the North American herb Arabidopsis lyrata, which is normally self-incompatible, with a low frequency of self-compatible plants. However, a few populations have become fixed for self-compatibility and have high selfing rates. Under greenhouse conditions, we estimated mean inbreeding depression per seed (based on cumulative vegetative performance calculated as the product of germination, survival and aboveground biomass) to be 0.34 for six outcrossing populations, and 0.26 for five selfing populations. Exposing plants to drought and inducing defences with jasmonic acid did not magnify these estimates. For outcrossing populations, however, inbreeding depression per seed may underestimate true levels of inbreeding depression, because self-incompatible plants showed strong reductions in seed set after (enforced) selfing. Inbreeding-depression estimates incorporating seed set averaged 0.63 for outcrossing populations (compared to 0.30 for selfing populations). However, this is likely an overestimate because exposing plants to 5% CO2 to circumvent self-incompatibility to produce selfed seed might leave residual effects of self-incompatibility that contribute to reduced seed set. Nevertheless, our estimates of inbreeding depression were clearly lower than previous estimates based on the same performance traits in outcrossing European populations of A. lyrata, which may help explain why selfing could evolve in North American A. lyrata.
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Outcrossing
Outbreeding depression
Allee effect
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Abstract Transitions from outcrossing to selfing have been a frequent evolutionary shift in plants and clearly play a role in species divergence. However, many questions remain about the initial mechanistic basis of reproductive isolation during the evolution of selfing. For instance, how important are prezygotic pre-pollination mechanisms (e.g. changes in phenology and pollinator visitation) in maintaining reproductive isolation between newly arisen selfing populations and their outcrossing ancestors? To test whether changes in phenology and pollinator visitation isolate selfing populations of Arabidopsis lyrata from outcrossing populations, we conducted a common garden experiment with plants from selfing and outcrossing populations as well as their F1 hybrids. Specifically, we asked whether there was isolation between outcrossing and selfing plants and their F1 hybrids through differences in 1) the timing or intensity of flowering; and/or 2) pollinator visitation. We found that phenology largely overlapped between plants from outcrossing and selfing populations. There were also no differences in pollinator preference related to mating system. Additionally, pollinators preferred to visit flowers on the same plant rather than exploring nearby plants, creating a large opportunity for self-fertilization. Overall, this suggests that prezygotic pre-pollination mechanisms do not strongly reproductively isolate plants from selfing and outcrossing populations of Arabidopsis lyrata .
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Outcrossing
Reproductive isolation
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