Direct and indirect selection on floral pigmentation by pollinators and seed predators in a color polymorphic South African shrub

The coexistence of different color morphs is often attributed to variable selection pressures across space, time, morph frequencies, or selection agents, but the routes by which each morph is favored are rarely identified. In this study we investigated factors that influence floral color polymorphisms on a local scale in Protea, within which approximately 40% of species are polymorphic. Previous work shows that seed predators and reproductive differences likely contribute to maintaining polymorphism in four Protea species. We explored whether selection acts directly or indirectly on floral color in two populations of Protea aurea, using path analysis of pollinator behavior, nectar production, seed predation, color, morphology, and maternal fecundity fitness components. We found that avian pollinators spent more time on white morphs, likely due to nectar differences, but that this had no apparent consequences for fecundity. Instead, the number of flowers per inflorescence underpinned many of the reproductively important differences between color morphs. White morphs had more flowers per inflorescence, which itself was positively correlated with nectar production, seed predator occurrence, and total long-term seed production. The number of seeds per plant to survive predation, in contrast, was not directly associated with color or any other floral trait. Thus, although color differences may be associated with conflicting selection pressures, the selection appears to be associated with the number of flowers per inflorescence and its unmeasured correlates, rather than with inflorescence color itself.     

Herbivores and plant defences affect selection on plant reproductive traits more strongly than pollinators

Pollinators and herbivores can both affect the evolutionary diversification of plant reproductive traits. However, plant defences frequently alter antagonistic and mutualistic interactions, and therefore, variation in plant defences may alter patterns of herbivore‐ and pollinator‐mediated selection on plant traits. We tested this hypothesis by conducting a common garden field experiment using 50 clonal genotypes of white clover (Trifolium repens) that varied in a Mendelian‐inherited chemical antiherbivore defence—the production of hydrogen cyanide (HCN). To evaluate whether plant defences alter herbivore‐ and/or pollinator‐mediated selection, we factorially crossed chemical defence (25 cyanogenic and 25 acyanogenic genotypes), herbivore damage (herbivore suppression) and pollination (hand pollination). We found that herbivores weakened selection for increased inflorescence production, suggesting that large displays are costly in the presence of herbivores. In addition, herbivores weakened selection on flower size but only among acyanogenic plants, suggesting that plant defences reduce the strength of herbivore‐mediated selection. Pollinators did not independently affect selection on any trait, although pollinators weakened selection for later flowering among cyanogenic plants. Overall, cyanogenic plant defences consistently increased the strength of positive directional selection on reproductive traits. Herbivores and pollinators both strengthened and weakened the strength of selection on reproductive traits, although herbivores imposed ~2.7× stronger selection than pollinators across all traits. Contrary to the view that pollinators are the most important agents of selection on reproductive traits, our data show that selection on reproductive traits is driven primarily by variation in herbivory and plant defences in this system.     

Direct and indirect effects of invasions of predators on a multiple-species community

A Lotka-Volterra system for a multiple species community with two trophic levels is analyzed to illustrate how community structure is reorganized upon invasions of predators. The lower trophic level is assumed to consist of interfering competing species, some of which are preferentially consumed by invading predators. Effects of invading predators on the lower trophic level are investigated in terms of predator-mediated coexistence and predator-induced instability. Competitive interactions between species in the lower trophic level result in indirect mutualism or indirect competition between predators depending on which competitors are preyed upon.     

Divergence on floral traits and vertebrate pollinators of two endemic Encholirium bromeliads

Shifts in pollen vectors favour diversification of floral traits, and differences in pollination strategies between congeneric sympatric species can contribute to reproductive isolation. Divergence in flowering phenology and selfing could also reduce interspecific crossing between self‐compatible species. We investigated floral traits and visitation rates of pollinators of two sympatric Encholirium species on rocky outcrops to evaluate whether prior knowledge of floral characters could indicate actual pollinators. Data on flowering phenology, visitation rates and breeding system were used to evaluate reproductive isolation. Flowering phenology overlapped between species, but there were differences in floral characters, nectar volume and concentration. Several hummingbird species visited flowers of both Encholirium spp., but the endemic bat Lonchophylla bokermanni and an unidentified sphingid only visited E. vogelii. Pollination treatments demonstrated that E. heloisae and E. vogelii were partially self‐compatible, with weak pollen limitation to seed set. Herbivores feeding on inflorescences decreased reproductive output of both species, but for E. vogelii the damage was higher. Our results indicate that actual pollinators can be known beforehand through floral traits, in agreement with pollination syndromes stating that a set of floral traits can be associated with the attraction of specific groups of pollinators. Divergence on floral traits and pollinator assemblage indicate that shifts in pollination strategies contribute to reproductive isolation between these Encholirium species, not divergence on flowering phenology or selfing. We suggest that hummingbird pollination might be the ancestral condition in Encholirium and that evolution of bat pollination made a substantial contribution to the diversification of this clade.     

Morph‐specific selection on floral traits in a polymorphic plant

Correlations between phenotypic traits are common in many organisms, but the relative importance of nonadaptive mechanisms and selection for the evolution and maintenance of such correlations are poorly understood. In polymorphic species, morphs may evolve quantitative differences in additional characters as a result of morph‐specific selection. The perennial rosette herb Primula farinosa is polymorphic for scape length. The short‐scaped morph is less damaged by grazers and seed predators but is more strongly pollen limited than the long‐scaped morph. We examined whether morph‐specific differences in biotic interactions are associated with differences in selection on two other traits affecting floral display (number of flowers and petal size) and on one trait likely to affect pollination efficiency (corolla tube width) in three P. farinosa populations. Differences in selection between morphs were detected in one population. In this population, selection for more flowers and larger petals was stronger in the short‐scaped than in the long‐scaped morph, and although there was selection for narrower corolla tubes in the short‐scaped morph, no statistically significant selection on corolla tube width could be detected in the long‐scaped morph. In the study populations, the short‐scaped morph produced more and larger flowers and wider corolla tubes. Current morph‐specific selection was thus only partly consistent with trait differences between morphs. The results provide evidence of morph‐specific selection on traits associated with floral display and pollination efficiency, respectively.     

Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study

1.  There are myriad ways in which pollinators and herbivores can interact via the evolutionary and behavioural responses of their host plants.
2.  Given that both herbivores and pollinators consume and are dependent upon plant-derived nutrients and secondary metabolites, and utilize plant signals, plant chemistry should be one of the major factors mediating these interactions.
3.  Here we build upon a conceptual framework for understanding plant-mediated interactions of pollinators and herbivores. We focus on plant chemistry, in particular plant volatiles and aim to unify hypotheses for plant defence and pollination. We make predictions for the evolutionary outcomes of these interactions by hypothesizing that conflicting selection pressures from herbivores and pollinators arise from the constraints imposed by plant chemistry.
4.  We further hypothesize that plants could avoid conflicts between pollinator attraction and herbivore defence through tissue-specific regulation of pollinator reward chemistry, as well as herbivore-induced changes in flower chemistry and morphology.
5.  Finally, we test aspects of our predictions in a case study using a wild tomato species, Solanum peruvianum , to illustrate the diversity of tissue-specific and herbivore-induced differences in plant chemistry that could influence herbivore and pollinator behaviour, and plant fitness.     

Indirect effects of grazing intensity on pollinators and floral visitation

1. The introduction of livestock in natural areas is a common disturbance that affects both plant and pollinator diversity and might affect their interaction. Understanding whether livestock affect a food resource for pollinators (i.e. flower abundance) and/or a pollinator assemblage (i.e. abundance and richness) has important implications for plant–pollinator interactions and still needs deeper investigation. 2. This study investigated how pollinator communities and flower abundance determined floral visitation frequency along a grazing gradient, using seven large paddocks in Patagonian Monte Desert that varied in livestock densities. Pollinator visitation frequency was measured in five of the most abundant native plant species of the region, present in all the paddocks, but that differed in reproductive strategy ranging from insect‐pollinated self‐compatible and self‐incompatible to wind‐pollinated. The influence of livestock density, insect, and flower abundance on visitation frequency was evaluated using D‐separation hierarchical path models. 3. Intermediate stocking densities showed the highest insect richness and abundance. Livestock density showed a negative quadratic relationship with insect richness; hymenopterans being the main insect group in the region. Flower density decreased with the increase in livestock density. The five plant species shared several pollinator species although each one supported a distinct assemblage. 4. The path model showed that livestock was not directly associated with pollinator visitation frequency; however, this apparent lack of association was as a result of opposite forces acting together. An increase in livestock density reduced visitation frequency through a decrease in insect abundance, yet, livestock simultaneously increased the pollinator visitation rate through decreased flower abundance. 5. This study describes how changes in the density of exotic mammals can affect pollinator and flower abundance, resulting in contrasting effects on flower visitation rates with, apparently, neutral net consequences. This illustrates the complexity of responses to plant–pollinator interactions to anthropogenic disturbances that alter the ecological context.     

Direct and indirect effects of predators on the dominant invertebrates of two freshwater littoral communities

Summary Two congeneric damselfly species, Enallagma traviatum and E. aspersum, dominate the littoral macroinvertebrates of Bays Mountain Lake and of the adjacent fish-free Ecology Pond, respectively (northeastern Tennessee, USA). Extending previous experimental studies, we test seven hypotheses concerning the role of fish (bluegill sunfish, Lepomis macrochirus) and larvaldragonfly (Anax junius) predation, competitive effects on damselflies, and the interaction between competition and predation, in determining invertebrate dominance in these communities. Three types of experiments were conducted: an enclosure experiment within Ecology Pond, an outdoor replicated tub experiment, and a laboratory behavior experiment. The in-situ enclosure experiment showed that E. traviatum larvae were more susceptible to Anax predation than were E. aspersum larvae; a tendency toward greater vulnerability to fish of E. aspersum compared with E. traviatum was not statistically significant. The outdoor tub experiment confirmed both of these trends with statistically significant results. In the tubs, both predators inhibited feeding of both zygopterans (as indicated by reduced fecal mass), particularly for E. aspersum in the presence of fish. This effect appears to have been primarily indirect, mediated through exploitation of the zooplankton. We also detected competitive effects of E. traviatum on E. aspersum: E. traviatum reduced the emergence and increased the exposure above the substrate of E. aspersum. In the absence of predators, E. traviatum inhibited feeding of E. aspersum via interference. In the laboratory behavior experiment, predators inhibited crawling by E. aspersum. E. aspersum was more exposed than was E. traviatum; it swam and crawled more than did E. traviatum, considerably increasing these movements at night. Over all, E. traviatum consistently appeared to be the more cryptic of the two species, and E. aspersum appeared to be much more active. Our results suggest an explanation for the clear difference in structure between communities like Bays Mountain Lake and Ecology Pond: predaceous fish eliminate large invertebrate predators and shift the community toward cryptic forms at relatively low densities, reflecting the effects of both predation and exploitation competition. In the absence of fish, large invertebrate predators are less able to deplete littoral invertebrates but may favor the more active forms, perhaps because these are better able to avoid invertebrate predators.     

Direct and indirect effects of plant genetic variation on enemy impact

Abstract.

• 1 The Tritrophic and Enemy Impact concepts predict that natural enemy impact varies: (a) among plant genotypes and (b) may depend on the abundance of heterospecific herbivores, respectively. I tested these predictions using three herbivore species on potted, cloned genotypes of Salik sericea Marshall in a common garden experiment.
• 2 Densities of the leaf miner (Phyllonorycter salicifoliella (Chambers)) and two leaf galling sawflies (Phyllocolpa nigrita (Marlatt) and Phyllocolpa eleanorae Smith and Fritz) varied significantly among willow clones, indicating genetic variation in resistance.
• 3 Survival and natural enemy impact caused by egg and larval parasitoids and/or unknown predators differed significantly among willow clones for each of the three herbivore species, indicating genetic variation in survival and enemy impact.
• 4 Survival of Phyllonorycter was negatively density-dependent among clones.
• 5 Survival of Phyllonorycter and Phyllocolpa eleanorae were positively correlated with densities of heterospecific herbivores among clones and parasitism of these species were negatively correlated with densities of the same heterospecific herbivores among clones.
• 6 At least for Phyllonorycter this positive correlation may suggest either facilitation of survival between herbivore species, which do not share natural enemies, or an apparent interaction caused by host plant genetic variation.
• 7 Among clones, egg parasitism of Phyllocolpa eleanorae was weakly positively correlated with density of Phyllocolpa nigrita. Since these species share the same Trichogramma egg parasitoid, this interaction could support the hypothesis of apparent competition.

     

Phenotypic selection on floral traits in the arctic plant Parrya nudicaulis (Brassicaceae)

The evolution of floral traits is often attributed to pollinator‐mediated selection; however, the importance of pollinators as selective agents in arctic environments is poorly resolved. In arctic and subarctic regions that are thought to be pollen limited, selection is expected to either favor floral traits that increase pollinator attraction or promote reproductive assurance through selfing. We quantified phenotypic selection on floral traits in two arctic and two subarctic populations of the self‐compatible, but largely pollinator‐dependent, Parrya nudicaulis. Additionally, we measured selection in plants in both open pollination and pollen augmentation treatments to estimate selection imposed by pollinators in one population. Seed production was found to be limited by pollen availability and strong directional selection on flower number was observed. We did not detect consistently greater magnitudes of selection on floral traits in the arctic relative to the subarctic populations. Directional selection for more pigmented flowers in one arctic population was observed, however. In some populations, selection on flower color was found to interact with other traits. We did not detect consistently stronger selection gradients across all traits for plants exposed to pollinator selection relative to those in the pollen augmentation treatment; however, directional selection tended to be higher for some floral traits in open‐pollinated plants.     

Selection on plant optical traits and floral scent: Effects via seed development and antagonistic interactions

Evolutionary explanations of plant reproductive traits have usually emphasized optical characteristics of plants and selection mediated by pollinators. In recent years, studies have been broadened by incorporating also interactions with antagonists and by studying plant fragrant cues. Here, we examined if optical and fragrance traits of the perennial herb Primula veris correlated with reproductive success, in terms of fruit and seed set, and with avoidance of seed predators. Selection path analysis showed that both optical and fragrance traits influenced total seed production, and effects occurred both via fruit and seed set and via predator avoidance. In one case the same trait, inflorescence height, influenced total seed production both positively and negatively through effects on different components of fitness. Our results lend support to the notion that selection by mutualists and antagonists simultaneously acts on optical and fragrance traits.     

Direct and indirect effects of masting on rodent populations and tree seed survival

Many plant species are thought to benefit from mast seeding as a result of increased seed survival through predator satiation. However, in communities with many different masting species, lack of synchrony in seed production among species may decrease seed survival by maintaining seed predator populations through the intermast cycle. Similarly, masting by different plant species may have different effects on the seed predator community. We conducted a three-year study in a northeastern USA temperate deciduous forest to determine if production of large seed crops by several tree species was synchronous, and if they had similar effects on all small mammal species. We found that red oak mast crops resulted in increased densities of Peromyscus leucopus and P. maniculatus , but had no effect on Clethrionomys gapperi abundance. Conversely, C. gapperi populations, but not Peromyscus populations, appeared to increase in response to a large red maple seed crop. Differences in small mammal abundance resulted in changes in species-specific seed survival: in the year of abundant C. gapperi , experimentally placed red oak acorns had significantly higher survival than in the year of high Peromyscus abundance. Red oak acorn removal was positively correlated with Peromyscus abundance, while red maple seed removal was significantly higher with increased C. gapperi abundance. Thus, species-specific seed production had differential effects on subsequent small mammal abundance, which in turn affected seed survival. We suggest that at the level of the community, even short-term lack of synchrony in production of large seed crops can cause variation in postdispersal seed survival, through differential effects on the community of small mammal seed predators.     

Direct and indirect causal effects of heterozygosity on fitness-related traits in Alpine ibex

Heterozygosity–fitness correlations (HFCs) are a useful tool to investigate the effects of inbreeding in wild populations, but are not informative in distinguishing between direct and indirect effects of heterozygosity on fitness-related traits. We tested HFCs in male Alpine ibex (Capra ibex) in a free-ranging population (which suffered a severe bottleneck at the end of the eighteenth century) and used confirmatory path analysis to disentangle the causal relationships between heterozygosity and fitness-related traits. We tested HFCs in 149 male individuals born between 1985 and 2009. We found that standardized multi-locus heterozygosity (MLH), calculated from 37 microsatellite loci, was related to body mass and horn growth, which are known to be important fitness-related traits, and to faecal egg counts (FECs) of nematode eggs, a proxy of parasite resistance. Then, using confirmatory path analysis, we were able to show that the effect of MLH on horn growth was not direct but mediated by body mass and FEC. HFCs do not necessarily imply direct genetic effects on fitness-related traits, which instead can be mediated by other traits in complex and unexpected ways.     

Natural selection on inflorescence color polymorphisms in wild Protea populations: The role of pollinators, seed predators, and intertrait correlations

? Premise of the study: The processes maintaining flower color polymorphisms have long been of evolutionary interest. Mechanistic explanations include selection through pollinators, antagonists, local environments, drift, and pleiotropic effects. We examined the maintenance of inflorescence color polymorphisms in the genus Protea (Proteaceae) of South Africa, in which ～40% of species contain different color morphs. ? Methods: We studied 10 populations of four bird-pollinated Protea species and compared adult performance, floral and leaf morphology, vegetative pigmentation, germination, and seedling survival between co-occurring pink and white morphs. We also tested for differences in pollination success and pre-dispersal seed predation. ? Key results: White morphs produced seeds 10% heavier and 3.5 times more likely to germinate, which all else being equal, should fuel positive selection on white. In one studied population per species, however, white morphs were more susceptible to seed predation by endophagous larvae. Pollinators had no morph-specific effects on female fecundity, as measured by amount or probability of seed set. Differences in stem color indicated that white morphs produced smaller quantities of pigment and associated compounds throughout, possibly explaining their higher seed palatability. ? Conclusions: Our findings suggest a mechanism for some white protea polymorphisms: deleterious pleiotropic effects on pink morphs are occasionally offset by reduced losses to seed-eating larvae. Because trends were repeated across species, we suggest that similar processes may also occur in other proteas, placing a new emphasis on seed predators for influencing some of South Africa's amazing floral diversity.     

The contribution of parasitism to selection on floral traits in Heuchera grossulariifolia

Parasites are ubiquitous and have well-documented ecological consequences. In contrast, the extent to which parasites drive phenotypic evolution in hosts remains obscure. We use a recently developed statistical technique--selective source analysis--to analyse the strength of phenotypic selection acting on floral traits in the plant Heuchera grossulariifolia attributable to attack by the seed-parasitic moth, Greya politella. This analysis spanned 3 years and included two sympatric populations of the host plant H. grossulariifolia that differ in ploidy. Our analyses revealed that attack by G. politella contributed to phenotypic selection for flowering time and floral display size, favouring earlier flowering in the polyploid population, later flowering in the diploid population and increased floral display size in the polyploid population. Although selection imposed by parasite attack was generally quite weak, in one of the 3 years parasites generated a modestly strong selection gradient (beta = -0.059) that explained 38.6% of total observed phenotypic selection for earlier flowering in the polyploid population. Together, our results demonstrate parasites can generate significant phenotypic selection, but that such selection may be sporadic across populations and time.     

Effects of flower and seed predators and pollinators on fruit production in two sequentially flowering congeners

We examined spatial and temporal variability of understory herbaceousvegetation on opposing north- and south-facing slopes in an eastern deciduousold-growth forest in southeastern Ohio, USA. Secondly, we explored theinfluenceof sampling scale and analytical technique on our assessment of diversitypatterns. The influence of aspect and seasonality were examined at varyingsampling scales using observed richness, evenness, andH diversity measures, non-parametric richnessestimators, species-area curves, and SHE analysis. Herb layer composition,abundance, and diversity were strongly influenced by location (north slope vs.south slope), seasonal sampling period (April, June, August), and plot size(micro (2 m²)- vs. meso (70m²)-scale samples). Although north and south plots werecompositionally distinct, they followed similar courses of change through thegrowing season. Richness, evenness, and H diversitywere generally greater on the south plot whereas herbaceous abundance wasgreater on the north plot. Species composition and diversity showed markedphenological (temporal) changes, and comparison of diversity measures at micro-and meso-scales produced markedly different results. Minimum sample areas of150–200 m² were needed to evaluate micro-scalerichness in these species rich communities, suggesting that forest understoriesmay be frequently undersampled in ecological studies. Comparison of observedandestimated meso-scale richness also suggested underestimation of richness in thenorth plot, particularly earlier in the growing season. Thus, sample size,area,and time of sampling appear critical to assessment of diversity in spatiallyandtemporally variable communities such as herbaceous forest understories.     

Pollinators and seed predators generate conflicting selection on Dalechampia blossoms

Plant–pollinator relationships are often mediated by floral traits that advertise the presence or amount of rewards. However, herbivores may also use these traits to find their hosts. In Dalechampia scandens, we tested whether floral advertisements that attract pollinators were also used by seed predators, and whether this generated conflicting selection pressures. We studied the influence of natural variation in the size of showy bracts, amount of reward, and two shape traits on pollinator visitation, pollen arrival on stigmas, seed production and seed predation. We then built a multivariate fitness function for these traits to estimate selection generated by pollinators and seed predators. Blossoms with larger bracts were visited by bees more frequently and received more pollen on their stigmas. Seed predators laid more eggs on blossoms with larger bracts and also on blossoms later producing more seeds. Consequently, selection for larger bract size exerted by pollinators was counteracted by the selection exerted by seed predators. As a result, net selection on bract size tended to be stabilizing. Additionally, we found selection on traits that increased the rate of self‐pollination (assuming uniform seed quality). These results illustrate the importance of both mutualists and antagonists in floral evolution, as well as the value of taking an integrative approach to assessing selection on floral traits.