Antiherbivore defenses alter natural selection on plant reproductive traits

While many studies demonstrate that herbivores alter selection on plant reproductive traits, little is known about whether antiherbivore defenses affect selection on these traits. We hypothesized that antiherbivore defenses could alter selection on reproductive traits by altering trait expression through allocation trade‐offs, or by altering interactions with mutualists and/or antagonists. To test our hypothesis, we used white clover, Trifolium repens, which has a Mendelian polymorphism for the production of hydrogen cyanide—a potent antiherbivore defense. We conducted a common garden experiment with 185 clonal families of T. repens that included cyanogenic and acyanogenic genotypes. We quantified resistance to herbivores, and selection on six floral traits and phenology via male and female fitness. Cyanogenesis reduced herbivory but did not alter the expression of reproductive traits through allocation trade‐offs. However, the presence of cyanogenic defenses altered natural selection on petal morphology and the number of flowers within inflorescences via female fitness. Herbivory influenced selection on flowers and phenology via female fitness independently of cyanogenesis. Our results demonstrate that both herbivory and antiherbivore defenses alter natural selection on plant reproductive traits. We discuss the significance of these results for understanding how antiherbivore defenses interact with herbivores and pollinators to shape floral evolution.     

Geographic variation of reproductive traits and competition for pollinators in a bird‐pollinated plant

Geographic variation in the reproductive traits of animal‐pollinated plants can be shaped by spatially variable selection imposed by differences in the local pollination environment. We investigated this process in Babiana ringens (Iridaceae), an enigmatic species from the Western Cape region of South Africa. B. ringens has evolved a specialized perch facilitating cross‐pollination by sunbirds and displays striking geographic variation in perch size and floral traits. Here, we investigate whether this variation can be explained by geographic differences in the pollinator communities. We measured floral and inflorescence traits, and abiotic variables (N, P, C, and rainfall) and made observations of sunbirds in populations spanning the range of B. ringens. In each population, we recorded sunbird species identity and measured visitation rates, interfloral pollen transfer, and whether the seed set of flowers was pollen limited. To evaluate whether competition from co‐occurring sunbird‐pollinated species might reduce visitation, we quantified nectar rewards in B. ringens and of other co‐flowering bird‐pollinated species in local communities in which populations occurred. Variation in abiotic variables was not associated with geographical variation of traits in B. ringens. Malachite sunbirds were the dominant visitor (97% of visits) and populations with larger‐sized traits exhibited higher visitation rates, more between‐flower pollen transfer and set more seed. No sunbirds were observed in four populations, all with smaller‐sized traits. Sunbird visitation to B. ringens was not associated with local sunbird activity in communities, but sunbird visitation was negatively associated with the amount of B. ringens sugar relative to the availability of alternative nectar sources. Our study provides evidence that B. ringens populations with larger floral traits are visited more frequently by sunbirds, and we propose that visitation rates to B. ringens may be influenced, in part, by competition with other sunbird‐pollinated species.     

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.     

昆虫植食对植物有性生殖的影响

植物在个体发育的各个阶段都与不同的群落成员相互作用,如竞争的植物、有益的传粉者和敌对的植食动物。昆虫植食在各类生态系统中普遍存在,并可能对植物有性生殖产生各种影响。植食昆虫可通过对植物有性生殖结构的消耗直接对植物生殖产生影响,也可通过影响植物资源分配和花性状等改变传粉者服务,从而间接对植物有性生殖带来正面、负面或中性的影响。同一植物的植食昆虫和传粉者往往对植物的吸引性状 （如花大小、气味、颜色等）有相同的偏好,因此植食者与传粉者均能对植物有性生殖性状施加选择压力。本文从昆虫植食对植物有性生殖的直接影响、间接影响以及植食昆虫对植物有性生殖性状选择的影响三个方面进行综述,以期为昆虫植食和生物资源多样性保护相关研究提供参考。     

Induced defences alter the strength and direction of natural selection on reproductive traits in common milkweed

Evolutionary biologists have long sought to understand the ecological processes that generate plant reproductive diversity. Recent evidence indicates that constitutive antiherbivore defences can alter natural selection on reproductive traits, but it is unclear whether induced defences will have the same effect and whether reduced foliar damage in defended plants is the cause of this pattern. In a factorial field experiment using common milkweed, Asclepias syriaca L., we induced plant defences using jasmonic acid (JA) and imposed foliar damage using scissors. We found that JA‐induced plants experienced selection for more inflorescences that were smaller in size (fewer flowers), whereas control plants only experienced a trend towards selection for larger inflorescences (more flowers); all effects were independent of foliar damage. Our results demonstrate that induced defences can alter both the strength and direction of selection on reproductive traits, and suggest that antiherbivore defences may promote the evolution of plant reproductive diversity.     

Plant volatiles induced by herbivore eggs prime defences and mediate shifts in the reproductive strategy of receiving plants

Plants can detect cues associated with the risk of future herbivory and modify defence phenotypes accordingly; however, our current understanding is limited both with respect to the range of early warning cues to which plants respond and the nature of the responses. Here we report that exposure to volatile emissions from plant tissues infested with herbivore eggs promotes stronger defence responses to subsequent herbivory in two Brassica species. Furthermore, exposure to these volatile cues elicited an apparent shift from growth to reproduction in Brassica nigra, with exposed plants exhibiting increased flower and seed production, but reduced leaf production, relative to unexposed controls. Our results thus document plant defence priming in response to a novel environmental cue, oviposition‐induced plant volatiles, while also showing that plant responses to early warning cues can include changes in both defence and life‐history traits.     

A hurricane alters pollinator relationships and natural selection on an introduced island plant

Novel relationships between the floral morphology of introduced plants and the trophic morphology of native pollinators have been hypothesized to cause strong natural selection on both parties, but evidence for such selection is rare. We capitalized on a natural disturbance to examine selection on an introduced plant, Heliconia wagneriana, on the island of Dominica, before and after Hurricane Maria. Prior to the hurricane, female Anthracothorax jugularis hummingbirds, which have longer bills than males, were the main visitor to H. wagneriana, and directional selection on corolla length was insignificant. After the hurricane, shorter‐billed male A. jugularis were the main visitor to H. wagneriana. The absence of trait matching between a short‐billed pollinator and a long‐flowered plant resulted in directional selection for shorter flowers because males preferentially visited plants with shorter flowers. The amount of nectar removed by male A. jugularis was negatively associated with flower length, with flowers >53 mm containing nearly five times the nectar than flowers <53 mm. We estimate a roughly 75% decrease in the population size of A. jugularis, and results suggest the heaviest mortality occurred among short‐billed male hummingbirds and larger‐bodied individuals of both sexes, which would have higher nectar requirements and the most difficulty obtaining nectar. Our results indicate that hurricanes may alter relationships between plants and pollinators and that lack of trait matching resulting from such disturbances may lead to selection on both plant and pollinator.     

Effects of gene flow on phenotype matching between two varieties of Joshua tree (Yucca brevifolia; Agavaceae) and their pollinators

In animal‐pollinated plants, local adaptation to pollinator behaviour or morphology can restrict gene flow among plant populations; but gene flow may also prevent divergent adaptation. Here, we examine possible effects of gene flow on plant–pollinator trait matching in two varieties of Joshua tree (Agavaceae: Yucca brevifolia). The two varieties differ in strikingly in floral morphology, which matches differences in the morphology of their pollinators. However, this codivergence is not present at a smaller scale: within the two varieties of Joshua tree, variation in floral morphology between demes is not correlated with differences in moth morphology. We use population genetic data for Joshua tree and its pollinators to test the hypotheses that gene flow between Joshua tree populations is structured by pollinator specificity, and that gene flow within the divergent plant–pollinator associations ‘swamps’ fine‐scale coadaptation. Our data show that Joshua tree populations are structured by pollinator association, but the two tree varieties are only weakly isolated – meaning that their phenotypic differences are maintained in the face of significant gene flow. Coalescent analysis of gene flow between the two Joshua tree types suggests that it may be shaped by asymmetric pollinator specificity, which has been observed in a narrow zone of sympatry. Finally, we find evidence suggesting that gene flow among Joshua tree sites may shape floral morphology within one plant–pollinator association, but not the other.     

Temporal variation in selection on male and female traits in wild tree crickets

Understanding temporal variation in selection in natural populations is necessary to accurately estimate rates of divergence and macroevolutionary processes. Temporal variation in the strength and direction of selection on sex‐specific traits can also explain stasis in male and female phenotype and sexual dimorphism. I investigated changes in strength and form of viability selection (via predation by wasps) in a natural population of male and female tree crickets over 4 years. I found that although the source of viability stayed the same, viability selection affected males and females differently, and the strength, direction and form of selection varied considerably from year to year. In general, males experienced significant linear selection and significant selection differentials more frequently than females, and different male traits experienced significant linear selection each year. This yearly variation resulted in overall weak but significant convex selection on a composite male trait that mostly represented leg size and wing width. Significant selection on female phenotype was uncommon, but when it was detected, it was invariably nonlinear. Significant concave selection on traits representing female body size was observed in some years, as the largest and smallest females were preyed on less (the largest may have been too heavy for flying wasps to carry). Viability selection was significantly different between males and females in 2 of 4 years. Although viability selection via predation has the potential to drive phenotypic change and sexual dimorphism, temporal variation in selection may maintain stasis.     

Genetic variation, disequilibrium and natural selection on reproductive traits in Allium vineale

Bulbils and seeds collected from Allium vineale plants from natural populations were grown under uniform conditions. The bulbil-derived offspring represented the parental generation, whereas the seed-derived offspring represented the sexually produced offspring generation. Molecular markers were used to identify maternal genets. Variation in traits determining the allocation to sexual and asexual reproduction was partitioned among genets and ramet families in the parental and offspring generations. From observations of a release of genetic variation and slippage in the mean phenotype in the offspring generation, we inferred that there exists extensive genetic disequilibrium for reproductive traits in A. vineale populations, that most of the genetic variance is because of dominance effects, and that natural selection favours a reduced allocation to sexual reproduction. No genetic correlation between sexual and asexual allocation traits was found. We discuss the implications of these results with respect to the evolution of a mixed reproductive system in A. vineale.     

Pollen transfer in fragmented plant populations: insight from the pollen loads of pollinators and stigmas in a mass‐flowering species

Pollinator and/or mate scarcity affects pollen transfer, with important ecological and evolutionary consequences for plant reproduction. However, the way in which the pollen loads transported by pollinators and deposited on stigmas are affected by pollination context has been little studied. We investigated the impacts of plant mate and visiting insect availabilities on pollen transport and receipt in a mass‐flowering and facultative autogamous shrub (Rhododendron ferrugineum). First, we recorded insect visits to R. ferrugineum in plant patches of diverse densities and sizes. Second, we analyzed the pollen loads transported by R. ferrugineum pollinators and deposited on stigmas of emasculated and intact flowers, in the same patches. Overall, pollinators (bumblebees) transported much larger pollen loads than the ones found on stigmas, and the pollen deposited on stigmas included a high proportion of conspecific pollen. However, comparing pollen loads of emasculated and intact flowers indicated that pollinators contributed only half the conspecific pollen present on the stigma. At low plant density, we found the highest visitation rate and the lowest proportion of conspecific pollen transported and deposited by pollinators. By contrast, at higher plant density and lower visitation rate, pollinators deposited larger proportion of conspecific pollen, although still far from sufficient to ensure that all the ovules were fertilized. Finally, self‐pollen completely buffered the detrimental effects on pollination of patch fragmentation and pollinator failure. Our results indicate that pollen loads from pollinators and emasculated flowers should be quantified for an accurate understanding of the relative impacts of pollinator and mate limitation on pollen transfer in facultative autogamous species.     

Compensation to simulated insect leaf herbivory in wild cotton (Gossypium hirsutum): responses to multiple levels of damage and associated traits

• Identifying the mechanisms of compensation to insect herbivory remains a major challenge in plant biology and evolutionary ecology. Most previous studies have addressed plant compensatory responses to one or two levels of insect herbivory, and the underlying traits mediating such responses remain elusive in many cases.
• We evaluated responses associated with compensation to multiple intensities of leaf damage (0% control, 10%, 25%, 50%, 75% of leaf area removed) by means of mechanical removal of foliar tissue and application of a caterpillar (Spodoptera exigua) oral secretions in 3‐month‐old wild cotton plants (Gossypium hirsutum). Four weeks post‐treatment, we measured plant growth and multiple traits associated with compensation, namely: changes in above‐ and belowground, biomass and the concentration of nutrients (nitrogen and phosphorus) and non‐structural carbon reserves (starch and soluble sugars) in roots, stems and leaves.
• We found that wild cotton fully compensated in terms of growth and biomass allocation when leaf damage was low (10%), whereas moderate (25%) to high leaf damage in some cases led to under‐compensation. Nonetheless, high levels of leaf removal (50% and 75%) in most cases did not cause further reductions in height and allocation to leaf and stem biomass relative to low and moderate damage. There were significant positive effects of leaf damage on P concentration in leaves and stems, but not roots, as well as a negative effect on soluble sugars in roots.
• These results indicate that wild cotton fully compensated for a low level of leaf damage but under‐compensated under moderate to high leaf damage, but can nonetheless sustain growth despite increasing losses to herbivory. Such responses were possibly mediated by a re‐allocation of carbohydrate reserves from roots to shoots.

     

Non‐linear relationship between intensity of plant–animal interactions and selection strength

The shape of the relationship between intensity of biotic interactions and strength of selection is important for spatial variation in selection, but is little explored. We quantified interactions and selection in 69 populations of the short‐lived herb Primula farinosa. As predicted because of saturation and depletion effects, the strength of selection on a discrete and on a continuously varying floral display trait were in several cases significantly non‐linearly related to the mean intensity of mutualistic and antagonistic interactions. Strength of selection was strongest at low levels of fruit initiation and at high intensities of seed predation. Seed predation varied more among populations than did fruit initiation and could explain a larger proportion of the among‐population variation in strength of selection. Our results support the contention that interaction intensity affects selection strength, and suggests that for mutualistic and antagonistic interactions that can be saturated or depleted, this relationship is sometimes non‐linear.     

Phenological change in a spring ephemeral: implications for pollination and plant reproduction

Climate change has had numerous ecological effects, including species range shifts and altered phenology. Altering flowering phenology often affects plant reproduction, but the mechanisms behind these changes are not well‐understood. To investigate why altering flowering phenology affects plant reproduction, we manipulated flowering phenology of the spring herb Claytonia lanceolata (Portulacaceae) using two methods: in 2011–2013 by altering snow pack (snow‐removal vs. control treatments), and in 2013 by inducing flowering in a greenhouse before placing plants in experimental outdoor arrays (early, control, and late treatments). We measured flowering phenology, pollinator visitation, plant reproduction (fruit and seed set), and pollen limitation. Flowering occurred approx. 10 days earlier in snow‐removal than control plots during all years of snow manipulation. Pollinator visitation patterns and strength of pollen limitation varied with snow treatments, and among years. Plants in the snow removal treatment were more likely to experience frost damage, and frost‐damaged plants suffered low reproduction despite lack of pollen limitation. Plants in the snow removal treatment that escaped frost damage had higher pollinator visitation rates and reproduction than controls. The results of the array experiment supported the results of the snow manipulations. Plants in the early and late treatments suffered very low reproduction due either to severe frost damage (early treatment) or low pollinator visitation (late treatment) relative to control plants. Thus, plants face tradeoffs with advanced flowering time. While early‐flowering plants can reap the benefits of enhanced pollination services, they do so at the cost of increased susceptibility to frost damage that can overwhelm any benefit of flowering early. In contrast, delayed flowering results in dramatic reductions in plant reproduction through reduced pollination. Our results suggest that climate change may constrain the success of early‐flowering plants not through plant‐pollinator mismatch but through the direct impacts of extreme environmental conditions.     

A selection strategy in plant transformation based on antisense oligodeoxynucleotide inhibition

Antisense oligodeoxynucleotide (asODN) inhibition was developed in the 1970s, and since then has been widely used in animal research. However, in plant biology, the method has had limited application because plant cell walls significantly block efficient uptake of asODN to plant cells. Recently, we have found that asODN uptake is enhanced in a sugar solution. The method has promise for many applications, such as a rapid alternative to time‐consuming transgenic studies, and high potential for studying gene functionality in intact plants and multiple plant species, with particular advantages in evaluating the roles of multiple gene family members. Generation of transgenic plants relies on the ability to select transformed cells. This screening process is based on co‐introduction of marker genes into the plant cell together with a gene of interest. Currently, the most common marker genes are those that confer antibiotic or herbicide resistance. The possibility that traits introduced by selectable marker genes in transgenic field crops may be transferred horizontally is of major public concern. Marker genes that increase use of antibiotics and herbicides may increase development of antibiotic‐resistant bacterial strains or contribute to weed resistance. Here, we describe a method for selection of transformed plant cells based on asODN inhibition. The method enables selective and high‐throughput screening for transformed cells without conferring new traits or functions to the transgenic plants. Due to their high binding specificity, asODNs may also find applications as plant‐specific DNA herbicides.     

Impact of plant and aphid stress history on infestation in arugula plants

Plants can activate inducible defence mechanisms against pests, pathogens, or chemical elicitors, such as ozone, mediated by reactive oxygen species (ROS), particularly hydrogen peroxide (H₂O₂). An unfavourable balance between ROS production and the plant antioxidant capacity seems to be responsible for the resulting susceptibility of the plant to insect attack. Arugula plants [Eruca sativa Mill. (Brassicaceae)] and green peach aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), were used in this study to test the hypothesis that the growth of an aphid population depends on both plant and insect stress history. We investigated the impact of density and duration of a previous aphid infestation, and the time lag before re‐infestation, on aphid population growth. In a second experiment, we assessed the effect on aphid population growth of previous ozone exposure of arugula plants in open top chambers receiving a continuous O₃ fumigation of 100–120 p.p.b., 90 min per day during 3 days. A third experiment was conducted to study the effect of aphid density during a previous infestation on the population growth on an uninfested host. Both previous herbivory and ozone changed the oxidative status of plant tissues and facilitated aphid population growth, which increased with the duration and density of a previous infestation by aphids. Colonization success also depended on the aphids' own history. Aphids coming from high‐density populations and/or longer infestation periods produced larger populations on an (initially) uninfested plant. Pest outbreaks in a polluted environment might be expected to be modulated by the hosts' spatial‐temporal heterogeneity related to the ozone exposure and previous herbivory.     

Assessment of correlational selection on tolerance and resistance traits in a host plant–parasitic plant interaction

Resistance and tolerance are considered to be different plant strategies against disease. While resistance traits prevent hosts becoming parasitized or reduce the extent of parasitism, tolerance traits reduce the fitness-impact of parasitism on infected hosts. Theoretical considerations predict that in some circumstances mutual redundancy will give hosts with either high resistance or high tolerance a fitness advantage over hosts that exhibit both of these traits together. However, empirical evidence has provided mixed results. In this paper, I describe the pattern of phenotypic selection imposed by the holoparasitic mistletoe Tristerix aphyllus upon resistance (spine length) and tolerance (branching) traits in the cactus Echinopsis chilensis. Results indicate that branching was an efficient compensatory mechanism, reducing 75.5% of the fitness-impact attributable to parasitism. Even though both traits showed a negative correlation, as expected from the presence of allocation costs between strategies, no correlational selection coefficient was significant indicating that selection did not favor alternative combinations of traits. Consequently, I did not find evidence for selection promoting mutually exclusive defense strategies against the mistletoe, which suggests that tolerance and resistance traits may coexist stably in populations of E. chilensis.