The genetic dissection of floral pollination syndromes

A major factor in the evolution of the angiosperms is the adaptation of plants to animal pollinators. The specific morphology of a flower, its color, nectar composition and scent production can all contribute to reproductive success by attracting pollinators and by limiting out-crossing with other species. It has now become feasible to dissect the genetic basis of plant adaptation to different pollinators.     

Reproductive biology and pollination of Utricularia reniformis A.St.‐Hil. (Lentibulariaceae)

Utricularia reniformis is an endemic Brazilian carnivorous plant, most common in high‐altitude grasslands. Knowledge of the reproductive biology of U. reniformis is essential for planning conservation strategies, but it is currently poorly understood. Thus, we studied the floral morphology, floral biology, breeding system and pollination of this species. U. reniformis produces and stores nectar in the flower spur, a classic feature of bee‐pollinated flowers, and we recorded Xylocopa sp. and Bombus sp. as pollinators. Moreover, although it is self‐compatible it is an obligate animal‐pollinated species, as the sensitive stigma avoids self‐pollination. However, in natural conditions reproductive success is low due to the rarity of visits from pollinators. We suggest that the low reproductive success caused by a deficit of pollinators may affect gene flow, causing loss of genetic diversity in U. reniformis.     

高山植物繁殖策略的研究进展

高山地区通常被认为是陆地上最为极端的生境之一,但却拥有许多形态特化的植物和较高的物种多样性。高山植物如何在严酷的环境中实现成功繁殖,这一问题倍受研究者们的关注。本文综合了国内外高山植物在资源分配、花形态对非生物环境因子的响应、动物传粉及其适应机制、果实和种子及克隆繁殖等繁殖策略方面的文献。为应对低温多雨雪的恶劣环境,一些高山植物采取花向日性、花冠闭合及花序保温结构等繁殖策略。高山植物的传粉者类群也发生了改变,主要为蜂类和蝇类。熊蜂(Bombusspp.)传粉的高效性,减少了高山环境对植物传粉造成的不利影响。当传粉者不可得时,植物不仅通过延迟自交和自助自交等机制来提供繁殖保障,还借助克隆繁殖及其他传粉机制(风媒或风虫媒)来维持种群的繁衍。依赖动物传粉的高山植物,可以采取增加繁殖构件的资源分配、加大"广告"投入以及较大的花展示或较长的花寿命来提高传粉者的拜访几率,以及借助泛化的花结构和选择合适的开花时间等策略来提高繁殖成功率。此外,大部分高山植物产生干果且具有持久的种子库,有利于种子的传播以及种子寻找萌发及幼苗生长的最佳外界环境。在今后的研究中,可着重探讨以下几个问题:(1)非生物环境因子对花形态的选择;(2)季节变化与繁殖策略;(3)群落水平上植物与传粉者的关系;(4)高山生态系统对全球变暖的响应。     

The influence of distinct pollinators on female and male reproductive success in the Rocky Mountain columbine

Although there are many reasons to expect distinct pollinator types to differentially affect a plant's reproductive success, few studies have directly examined this question. Here, we contrast the impact of two kinds of pollinators on reproductive success via male and female functions in the Rocky Mountain columbine, Aquilegia coerulea . We set up pollinator exclusion treatments in each of three patches where Aquilegia plants were visited by either day pollinators (majority bumble bees), by evening pollinators (hawkmoths), or by both (control). Day pollinators collected pollen and groomed, whereas evening pollinators collected nectar but did not groom. Maternal parents, potential fathers and progeny arrays were genotyped at five microsatellite loci. We estimated female outcrossing rate and counted seeds to measure female reproductive success and used paternity analysis to determine male reproductive success. Our results document that bumble bees frequently moved pollen among patches of plants and that, unlike hawkmoths, pollen moved by bumble bees sired more outcrossed seeds when it remained within a patch as opposed to moving between patches. Pollinator type differentially affected the outcrossing rate but not seed set, the number of outcrossed seeds or overall male reproductive success. Multiple visits to a plant and more frequent visits by bumble bees could help to explain the lack of impact of pollinator type on overall reproductive success. The increase in selfing rate with hawkmoths likely resulted from the abundant pollen available in experimental flowers. Our findings highlighted a new type of pollinator interactions that can benefit a plant species.     

Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae)

Inga species present brush‐type flower morphology allowing them to be visited by distinct groups of pollinators. Nectar features in relation to the main pollinators have seldom been studied in this genus. To test the hypothesis of floral adaptation to both diurnal and nocturnal pollinators, we studied the pollination ecology of Inga sessilis, with emphasis on the nectar secretion patterns, effects of sequential removals on nectar production, sugar composition and the role of diurnal and nocturnal pollinators in its reproductive success. Inga sessilis is self‐incompatible and pollinated by hummingbirds, hawkmoths and bats. Fruit set under natural conditions is very low despite the fact that most stigmas receive polyads with sufficient pollen to fertilise all ovules in a flower. Nectar secretion starts in the bud stage and flowers continually secreting nectar for a period of 8 h. Flowers actively reabsorbed the nectar a few hours before senescence. Sugar production increased after nectar removal, especially when flowers were drained during the night. Nectar sugar composition changed over flower life span, from sucrose‐dominant (just after flower opening, when hummingbirds were the main visitors) to hexose‐rich (throughout the night, when bats and hawkmoths were the main visitors). Diurnal pollinators contributed less than nocturnal ones to fruit production, but the former were more constant and reliable visitors through time. Our results indicate I. sessilis has floral adaptations, beyond the morphology, that encompass both diurnal and nocturnal pollinator requirements, suggesting a complementary and mixed pollination system.     

How flower biology and breeding system affect the reproductive success of the narrow endemic Polygala vayredae Costa (Polygalaceae)

Polygala vayredae is a narrow endemic species from the oriental pre-Pyrenees. Despite its conservation status and rarity, no information is available on its reproductive biology. As the flower is the structure directly involved in pollinator attraction, its morphological and functional traits have major effects on the reproductive success of the plant. In this work, the flower biology and breeding system of P. vayredae were studied to evaluate how they affect the reproductive outcome in natural populations. Flower morphology, flower rewards, and male and female functioning throughout the lifespan of the flower were assessed. Pollination experiments, involving pollinator exclusion and pollen from different sources, were conducted, and the pollen ovule index was determined. Female fitness and the occurrence of pollen limitation were assessed in three natural populations over 2 years by observing the presence of pollen on the stigma, pollen tube development, and fruit production. Polygala vayredae flowers are elaborate and long-lived with nectar rewards. The floral traits are well adapted to xenogamy and entomophily, which are in accordance with the observed breeding system and auto-incompatibility system. No mechanism of reproductive assurance was observed and P. vayredae strictly depends on pollinators to set fruit. Low fruit production was observed in the studied populations, which was largely the result of scarce, unreliable, and/or inefficient pollinators and poor pollen quality. In addition, available resources may be a limiting factor. The reproductive strategy of P. vayredae prevents inbreeding depression by a self-incompatibility system, which in years of scarce pollinators is overcome by the plant habit.  © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society , 2008, 157 , 67–81.     

Mecardonia tenella (Plantaginaceae) Attracts Oil-, Perfume-, and Pollen-Gathering Bees in Southern Brazil

Floral characteristics often indicate the pollinators' functional group visiting the plant and the pollination syndromes associated with them. This idea has been challenged in the past decades due to increasing evidence that most plants, including those exhibiting floral syndromes, are visited by large arrays of species that differ in their effectiveness as pollinators. Our study focuses on Mecardonia tenella (Plantaginaceae) from the Araucaria forest of southern Brazil, which exhibits characteristics of the oil flower pollination syndrome. However, it is visited by three types of functional groups of bees: male orchid bees, oil-collecting bees, and pollen-seeking bees. The relative contribution of each functional group to the plant's reproductive success was estimated based on their pollen load, visitation frequency, and morphology. We assessed resources, phenology, and breeding system of M. tenella . Our results indicate that flowers lack nectar, but volatiles, lipids, and pollen are resources that can be gathered by visitors. This combination of floral traits and visitors' assemblage makes M. tenella a challenge to the concept of pollination syndromes. Our findings indicate that the current interactions may not reflect the circumstances under which some floral traits of this plant were selected.     

Pollination, Flower Longevity, and Reproductive Biology of Gongora quinquenervis Ruíz and Pavón (Orchidaceae) in an Atlantic Forest Fragment of Pernambuco, Brazil

Abstract: The pollinators, flower longevity, and reproductive success of Gongora quinquenervis were studied in Refúgio Ecológico Charles Darwin, a preserved fragment of Atlantic Forest in Pernambuco. G. quinquenervis is epiphytic, and its flowers have osmophores, glands that produce aromatic volatiles, that are collected by males of Euglossini (Hymenoptera, Apidae). Every flower of an inflorescence opened simultaneously, however, overlaps in floral phases between individuals were low. Pollinaria deposition on the stigma caused immediate wilting of the perianth, while pollinaria removal had no influence on flower longevity. The reproductive system experiments showed that the species is self-compatible. The characteristics of floral morphology and its highly specialized pollination mechanism are efficient in limiting autogamy and geitonogamy and favouring cross-pollination. Three species of Euglossa were found ( E. cordata, E. perpulchra and an undescribed species) visiting the flowers of G. quinquenervis. All these efficiently removed the pollinaria of the flowers, which adhered to the posterior margin of the scutellum. Even though there was a high pollinaria removal rate by pollinators, the reproductive success in the field was extraordinarily low. We suggest that low fruit set, despite high pollinator frequency, is a result of a combination of the particular phonological characteristics of G. quinquenervis, such as short flower longevity and low overlap of flowering phases between individuals, leading to the reduced population of this orchid in the degraded Atlantic Forest. Conservation measures are necessary to guarantee the survival of G. quinquenervis in the northern part of the Atlantic Forest of Brazil.     

Functional differentiation in pollination processes among floral traits in Serapias species (Orchidaceae)

Floral displays, influencing attractiveness to insects, increase the number of pollinator visits and the efficiency of each visit in terms of pollen exchange and thus affect the plant reproductive success. Here, we conducted an in situ manipulation experiment to investigate whether the floral modifications affect reproductive success in natural orchid populations of Serapias lingua and Serapias vomeracea. We estimated male and female reproductive success of three treatment groups, disassembly of floral tube, cutting of lip, and painting of the callus surface, in terms of pollinaria removed/deposited and fruit production. Results revealed that phenotypic modification had opposite effects on reproductive success of two examine species. Indeed, reproductive success was significantly increased by the detached of the petals and sepals, and decreased, due to callus painting and lip removal, in S. lingua. On the contrary, unmanipulated plants of S. vomeracea showed significantly higher value of pollinaria removed and deposited and fruit set than manipulated ones. The differences between S. lingua and S. vomeracea agree to the different pollination strategy of examined species. S. vomeracea shows shelter imitation strategy, and thus, the disassembly of tunnel‐like corolla does not allow the insects to use the flower as a refuge, while S. lingua is a sexually deceptive orchid and therefore the opening of the flower made more visible callus (visible at a greater distance) increasing the pollinators attraction. This study provides evidence that pollinators were largely sensitive to the experimental modification of the flower phenotype, which is consistent with the presence of significant selection on individual floral characters. Our experimental investigations of the effects of variation in display on pollinator visitation provide insights into the evolution of floral morphology in orchid with shelter imitation strategy.     

Fruit production and floral traits: correlated evolution in <Emphasis Type="Italic">Govenia</Emphasis> (Orchidaceae)

The most common estimate of reproductive success in orchids is usually fruit set. Factors such as resource limitation and certain floral traits may influence reproductive success in animal-pollinated plants. Correlated evolution of reproductive success vs. seven floral traits (inflorescence length, flower number, flower distribution along inflorescence, dorsal sepal length, lateral sepal length, flower color, and column position) was studied in eight species of Govenia. Taxa represented three lineages in the genus. Independent contrasts were calculated on a phylogeny inferred from chloroplast (trnL-F IGS) DNA sequences, and a correlation test and multiple regression were then performed. Two data sets were evaluated, one including all eight species and another excluding G. utriculata, which is autogamous. The historical analyses showed that there is a correlation between reproductive success and dorsal sepal length, column position, and flower number, these correlations suggest that changes in these floral traits usually accompany evolutionary shifts in reproductive success. Multiple regression tests suggest that changes in reproductive success can be explained by shifts in flower number, inflorescence length, column position and by dorsal sepal length. When phylogeny is taken into account, our analyses showed that evolutionary shifts in these floral traits were correlated with changes in reproductive success. Evolutionary correlation between reproductive success and floral traits might be explained by the natural selection of certain floral phenotypes by pollinators.     

Fruit production in cranberry (Ericaceae: Vaccinium macrocarpon): a bet-hedging strategy to optimize reproductive effort

In the cultivated cranberry (Vaccinium macrocarpon), reproductive stems produce 1-3 fruit even though they usually have 5-7 flowers in the spring. We undertook experiments to test the hypothesis that this was an adaptive life history strategy associated with reproductive effort rather than simply the result of insufficient pollination. We compared fruit production on naturally pollinated plants with those that were either manually pollinated or that were caged to exclude insects. Clearly, insects are necessary for the effective pollination of cranberry plants, but hand pollination of all flowers did not result in an increase in fruit number. Most of the upper flowers, which had significantly fewer ovules than did the lower flowers, aborted naturally soon after pollination. However, when the lower flower buds were removed, the upper flowers produced fruit. This suggests that the upper flowers may serve as a backup if the earlier blooming lower ones are lost early in the season. Furthermore, the late-blooming flowers may still contribute to the plant's reproductive success as visiting pollinators remove the pollen, which could serve to sire fruit on other plants. These results are discussed in the context of their possible evolutionary and proximate causes.     

Anther evolution: pollen presentation strategies when pollinators differ

Male-male competition in plants is thought to exert selection on flower morphology and on the temporal presentation of pollen. Theory suggests that a plant's pollen dosing strategy should evolve to match the abundance and pollen transfer efficiency of its pollinators. Simultaneous pollen presentation should be favored when pollinators are infrequent or efficient at delivering the pollen they remove, whereas gradual dosing should optimize delivery by frequent and wasteful pollinators. Among Penstemon and Keckiella species, anthers vary in ways that affect pollen release, and the morphology of dried anthers reliably indicates how they dispense pollen. In these genera, hummingbird pollination has evolved repeatedly from hymenopteran pollination. Pollen production does not change with evolutionary shifts between pollinators. We show that after we control for phylogeny, hymenopteran-adapted species present their pollen more gradually than hummingbird-adapted relatives. In a species pair that seemed to defy the pattern, the rhythm of anther maturation produced an equivalent dosing effect. These results accord with previous findings that hummingbirds can be more efficient than bees at delivering pollen.     

BREEDING SYSTEM EVOLUTION IN LEAVENWORTHIA: BREEDING SYSTEM VARIATION AND REPRODUCTIVE SUCCESS IN NATURAL POPULATIONS OF LEAVENWORTHIA CRASSA (CRUCIFERAE)

Populations of Leavenworthia crassa (Cruciferae) studied for 3 years exhibited among- and within-population genetic variation for a suite of floral and reproductive traits (flower width, petal length, anther position, ability to set seeds in the absence of pollinators, time to first flowering) associated with breeding system. We used electrophoretic markers to show that a population with small, monomorphically colored flowers with introrse anthers had a significantly lower outcrossing rate (t = 0.03) than did a population with larger, polymorphically colored flowers with extrorse anthers (t = 0.33). In the more-outcrossing population the correlation between higher maternal plant outcrossing rate and the suite of six traits approached significance (P < 0.067), with greater petal size, greater flower width, and reduced ability to set seeds in the absence of pollinators contributing significantly. Plants in selfing populations had a generally higher reproductive success, with a higher number of flowers per plant, a smaller proportion of unfertilized ovules, a smaller proportion of fertilized ovules aborted, a higher rate of fruit set, and overall a larger number of seeds matured than did plants from the more outcrossing populations. Pollen limitation did not appear to account for lower reproductive success in outcrossing populations. Resource limitation did not differ substantially between populations. However, within-ovary patterns of fertilization, abortion, and seed weight were significantly less random in outcrossing populations than in selfing populations, suggesting that differential gamete and embryo success may be responsible for lower reproductive success in outcrossing populations.     

The Classification and Functional Significance of Staminodes in Angiosperms

All staminodes in an androecium fail to produce viable pollen grains and cannot contribute directly to male fitness. Staminodes are identified in the flowers of approximately 54% of known genera representing >32% of all angiosperm families. The functional morphology and biochemistry of staminodes differs significantly from stamens with fertile anthers. In the absence of sperm production, some staminodes evolved novel adaptations contributing to the reproductive success of their flowers. We subdivided these staminodes into eight functional types: 1) Staminodes offering visual/olfactory cues; 2) Staminodes offering edible/inedible rewards; 3) Staminodes that deceive pollinators with false rewards; 4) Staminodes facilitating or directing the movements of pollinators in flowers;5) Stami nodes that facilitate stigma movement; 6) Staminodes functioning as secondary pollen presenters; 7) Staminodes that protect other floral organs; 8) Staminodes that prevent mechanical self pollination (autogamy). As a component within a flower, the majority of staminodes function as promoters of reproductive success by interacting directly with the pollinator to increase pollination efficiency (both pollen dispersal and deposition). Therefore, it is not surprising that one staminode may have more than one function over the flower′s lifespan and is closely associated with the size, abundance, behavior and taxonomic diversity of pollinators, floral predators and thieves. To correctly evaluate the function of staminodes, multi disciplinary approach using a range of protocols, equipment and materials is suggested. This approach allows us to compare the roles different staminodes play in the reproductive success of both closely and distantly related angiosperms, then uncover their evolutionary significance in angiosperm diversification.     

Pollination of the European food-deceptive Traunsteinera globosa (Orchidaceae): the importance of nectar-producing neighbouring plants

European food-deceptive orchids generally flower early in spring and rely on naïve pollinators for their reproduction. Some species however, flower later in the summer, when many other rewarding plants species are also in bloom. In dense flowering communities, deceptive orchids may suffer from competition for pollinator resources, or might alternatively benefit from higher community attractiveness. We investigated the pollination strategy of the deceptive species Traunsteinera globosa, and more specifically whether it benefited from the presence of coflowering rewarding species. We carried out a population survey to quantify the density and reproductive success of the orchid as well as the density of all coflowering species. Our results suggest that the deceptive orchid not only benefited from the presence of coflowering species, but that interestingly the density of the species Trifolium pratense was significantly positively correlated with the orchid's reproductive success. This species might simply act as a magnet species attracting pollinators near T. globosa, or could influence the orchid reproductive fitness through a more species-specific interaction. We propose that morphological or colour similarities between the two species should be investigated in more detail to decipher this pollination facilitation effect.     

Floral color change in Weigela middendorffiana (Caprifoliaceae): reduction of geitonogamous pollination by bumble bees

We examined the significance of retaining color-changed flowers in pollination success of Weigela middendorffiana through a single visit of bumble bees. Inner parts of flowers changed color with age from yellow to red. In an investigation of the mating system, duration of each color phase, reproductive ability of each of the color-phase flowers, and the effects of color-changed flowers on bumble bee behavior (1) flowers of this species were self-incompatible, (2) color-changed flowers provided little reward to pollinators and little residual reproductive ability, (3) the timing of floral color change was delayed with the progress of flowering season within individual plants, while the duration of the red phase shortened with the progress of flowering season, and (4) red-phase flowers did not attract bumble bees at a distance but did contribute to reducing the number of successive flower visits during a single stay within the plants. Red-phase flowers seemed to indicate the low reward level of old flowers and functioned as a cue to discourage pollinators from staying longer on the same plant. Our results predict that the retention of color-changed flowers without sexual function can enhance the pollination success of a whole plant through male function by reducing successive flower visits during a single stay of pollinators, i.e., geitonogamous pollination.     

Pollination effectiveness and pollen dispersal in a Rhododendron ferrugineum (Ericaceae) population

Many alpine plants are predominantly outcrossing, thus plant reproductive success is highly dependent on effectiveness of pollinators. How pollinators transfer pollen from one flower to another is of great interest in understanding the genetic structure in plant populations. We studied (1) the role and effectiveness of insect visitors for pollination, and (2) their contribution as pollen vectors for gene dispersal in a Rhododendron ferrugineum population. Various insect visitors were recorded, including Hymenoptera, Diptera, Coleoptera, and Lepidoptera. The most frequent and effective insects were honey bees and bumblebees. Muscid flies were considered as important pollinators, particularly due to their relatively high visitation rate. Syrphid flies, Formicidae, and Coleoptera were ineffective in transporting pollen, while the effectiveness of Lepidoptera and Empididae was negligible. A fluorescence labelling experiment revealed that pollen dispersal was restricted (0 - 2 m) in a dense R. ferrugineum stand and decreased in a leptokurtic fashion. This might lead to geitonogamous self-pollination that could explain the close relationship between individuals found in genetic studies of R. ferrugineum. However, some pollen grains may travel 40 - 45 m, which implies the occurrence of cross-pollination through the foraging activities of bumblebees and honey bees.     

Reproductive success of Dactylorhiza incarnata ssp. incarnata (Orchidaceae): the effects of population size and plant visibility

Reproduction of plants pollinated solely by flower-visiting animals depends on the ability of the population and each of its flowering member to attract pollinators. Factors affecting the pollination of nectarless species differ somewhat from those affecting the pollination of rewarding species due to the avoidance behaviour of pollinators after visiting empty flowers.
We studied a non-mimic food-deceptive orchid, Dactylorhiza incarnata ssp. incarnata, in 16 populations in central Finland to examine if population properties and plant size affected reproductive success of plants.
We found that the number of flowering plants increased total pollinia removal and seed production of the population, but had no effect on reproduction of individual plants. Dactylorhiza incarnata occurred in open mires with virtually no rewarding species in the neighbourhood, but the distance from the forest edge did not have any effect on reproduction. However, increased variation in the number of flowers among within-population plants enhanced plant reproductive success. The increased variation probably hampered the learning process of flower visitors. Plant size affected reproductive success only in populations with a high general reproductive success indicating that in the rarely visited populations, pollination of individual plants is mainly affected by random effects.     

Nectar secretion dynamic links pollinator behavior to consequences for plant reproductive success in the ornithophilous mistletoe Psittacanthus robustus

The mistletoe Psittacanthus robustus was studied as a model to link flower phenology and nectar secretion strategy to pollinator behaviour and the reproductive consequences for the plant. The bright‐coloured flowers presented diurnal anthesis, opened asynchronously throughout the rainy season and produced copious dilute nectar as the main reward for pollinators. Most nectar was secreted just after flower opening, with little sugar replenishment after experimental removals. During the second day of anthesis in bagged flowers, the flowers quickly reabsorbed the offered nectar. Low values of nectar standing crop recorded in open flowers can be linked with high visitation rates by bird pollinators. Eight hummingbirds and two passerines were observed as potential pollinators. The most frequent flower visitors were the hummingbirds Eupetomena macroura and Colibri serrirostris, which actively defended flowering mistletoes. The spatial separation between anthers, stigma and nectar chamber promotes pollen deposition on flapping wings of hovering hummingbirds that usually probe many flowers per visit. Seed set did not differ between hand‐, self‐ and cross‐pollinated flowers, but these treatments set significantly more seeds than flowers naturally exposed to flower visitors. We suggest that the limitation observed in the reproductive success of this plant is not related to pollinator scarcity, but probably to the extreme frequency of visitation by territorial hummingbirds. We conclude that the costs and benefits of plant reproduction depend on the interaction strength between flowers and pollinators, and the assessment of nectar secretion dynamics, pollinator behaviour and plant breeding system allows clarification of the complexity of such associations.     

Pollinator behavior and deceptive pollination: learning process and floral evolution

Some species of flowering plants engage in nonmodel deceptive pollination, attracting pollinators by large nonmimetic floral displays and providing no reward. Pollinators can learn to avoid deceptive plants and to favor nectariferous species. The reproductive success of these species is expected to be density dependent for two opposite reasons: the commoner cheating flowers are, the easier they are to avoid and the lower the quality of the patch, making it more difficult to recognize that unrewarding flowers are not profitable. When a deceptive species is made up of multiple floral variants, pollinators' learning could decrease the reproductive success of any particularly common floral variant. Within a population of deceptive plants, mean reproductive success could, therefore, vary with the number of floral variants. We investigate these three hypotheses by modeling the behavior of pollinators foraging in communities of deceptive and rewarding flowers. Simulations revealed that the reproductive success of deceptive flowers varies in a density-dependent manner and that floral variants can be submitted to negative frequency-dependent selection. We compare density dependence in nonmodel deceptive species to what is expected in Batesian mimics and discuss possible selection of morphological variants. Finally, we survey how pollinators' learning capacities can make mean reproductive success depend on morphological variability within a population.