Because inbreeding, herbivory, and disease are common in plants and their separate impacts on fitness are well documented, investigators have begun to examine the consequences of inbreeding on plant-herbivore and plant-pathogen interactions. In this study, we examined the interrelationships among inbreeding, herbivory, and disease on reproductive output through both male (pollen production and pollen performance) and female (fruit and seed production and seed germination) functions. Inbred (selfed) and outbred plants from five families of a wild gourd (Cucurbita pepo ssp. texana) were grown in five 0.2-ha randomized blocks in an experimental garden. Half of the inbred and half of the outbred plants were sprayed weekly with a contact pesticide to control herbivores. The other half of the plants served as the controls (no-spray treatment). The spray treatment significantly reduced damage by cucumber beetles and aphid infestation levels, the two primary herbivores of the wild gourd. Moreover, because these herbivores are the sole vectors for the five most common viral diseases of cucurbits (Watermelon mosaic-2, Cucumber mosaic, Zucchini yellow mosaic, Papaya ringspot, and Squash mosaic), the spray treatment also significantly reduced the amount and severity of the symptoms of viral diseases. Our analyses reveal that (1) there is variation for resistance to herbivores and pathogens among the five families used in the study, indicating that there is broad-sense heritability for resistance; (2) inbred plants suffer greater herbivore damage and have more symptoms of viral infection than outbred plants, i.e., there is inbreeding depression for herbivore/pathogen resistance; (3) the impacts of insecticide applications and inbreeding on reproduction are mostly additive; (4) both male and female functions are significantly affected by the spray treatment and inbreeding; and (5) the adverse effects of both inbreeding and the increased exposure to herbivores/pathogens in the no-spray treatment are greater for female function than for male function, indicating that the impact of genetic and environmental stress can differentially affect the two sexual functions. Together, these findings have important implications for the evolution of selfing, the conservation of small populations, and the establishment and transmission of diseases within populations.
For species with bicellular pollen, the attrition of pollen tubes is often greatest where the style narrows at the transition between stigmatic tissue and the transmitting tissue of the style. In this region, the tubes switch from predominantly autotrophic to predominantly heterotrophic growth, the generative cell divides, the first callose plugs are produced, and, in species with RNase-type self-incompatibility (SI), incompatible tubes are arrested. We review the literature and present new findings concerning the genetic, environmental and stylar influences on the performance of pollen before and during the autotrophic-heterotrophic transition of pollen tube growth. We found that the ability of the paternal sporophyte to provision its pollen during development significantly influences pollen performance during the autotrophic growth phase. Consequently, under conditions of pollen competition, pollen selection during the autotrophic phase is acting on the phenotype of the paternal sporophyte. In a field experiment, using Cucurbita pepo, we found broad-sense heritable variation for herbivore-pathogen resistance, and that the most resistant families produced larger and better performing pollen when the paternal sporophytes were not protected by insecticides, indicating that selection during the autotrophic phase can act on traits that are not expressed by the microgametophyte. In a study of a weedy SI species, Solanum carolinense, we found that the ability of the styles to arrest self-pollen tubes at the autotrophic-heterotrophic transition changes with floral age and the presence of developing fruits. These findings have important implications for selection at the level of the microgametophyte and the evolution of mating systems of plants.
Each inflorescence on Lotus corniculatus commonly aborts about half of its immature fruits. Compared to random patterns of fruit abortion, natural patterns of fruit abortion produce mature fruits that contain significantly more seeds. Moreover, these progeny are more likely to germinate, are more vigorous as seedlings, and have greater reproductive output as adults. These results indicate that L. corniculatus selectively aborts those fruits with the fewest seeds and, by doing so, increases the average quality of its offspring.
The pollen competition hypothesis predicts that when the number of pollen grains deposited onto stigmas exceeds the number of ovules, selection can operate in the time frame between deposition and fertilization. Moreover, because of the overlap in gene expression between the two phases of the life cycle, selection on microgametophytes may alter the resulting sporophytic generation. The extent to which pollen competition occurs in nature has been unclear, because tests of the predictions of the pollen competition hypothesis have used cultivars and/or artificial growth conditions and hand‐pollination techniques. In this study we used a wild species, Cucurbita foetidissima, in its natural habitat (southern New Mexico) to determine the amount and timing of the arrival of pollen onto stigmas, the relationship between pollen deposition and seed number, and the effects of the intensity of pollen competition on progeny vigor. We found that ∼900 pollen grains are necessary for full seed set and that a single visit by a pollinator results in the deposition of 653.0 ± 101.8 pollen grains. About 29% of the flowers receiving a single pollinator visit had 900 or more pollen grains on its stigma. Moreover, within 2 h of anthesis, >4000 pollen grains were deposited onto a typical stigma, indicating that multiple pollinator visits must have occurred. Fruits produced by multiple visits had greater seed numbers (206 vs. 147) than fruits produced by a single visit. Finally, the progeny produced by multiple pollinator visits were more vigorous than those produced by single visits with respect to five measures of vegetative growth (MANCOVA, Wilks’ lambda = 0.96, F6,370 = 2.54, P < 0.02. These data demonstrate that conditions for pollen competition exist in nature and support the prediction that pollen competition enhances offspring vigor.
We used an F1 hybrid of zucchini and its wild progenitor to examine the effects of pollen competition on progeny performance. We experimentally varied the intensity of pollen competition by depositing large or small pollen loads onto stigmas. To separate the effects of pollen competition from maternal effects, we excised the styles of flowers receiving the large pollen loads after only the fastest pollen tubes had entered the ovary. The styles from flowers receiving small pollen loads were excised after both fast- and slow-growing tubes had entered the ovary. Consequently, the mature fruits from the two treatments were similar in seed number and weight. Because our previous studies had revealed that fast- and slow-growing pollen tubes fertilize ovules in different regions (locations) within the ovary (fast into region I and slow into region 3), we examined the vigor of the progeny produced in regions I and 3 from both large and small pollen loads. The results revealed that the progeny from large pollen loads outperform progeny from small pollen loads. We also found that for small pollen loads, the progeny from region I outperform the progeny from region 3, which indicates that the progeny produced by the fastest pollen tubes outperform the progeny produced from the slowest.
In a series of field experiments Diabrotica beetle herbivory was found to influence the magnitude of inbreeding depression in Cucurbita pepo ssp. texana, an annual monoecious vine. Beetles damage flowers and fruits and chew dime-sized holes in leaf tissue between major veins. Inbred plants were found to be more likely to be damaged by beetles and to have more leaves damaged per plant than outcrossed plants. A positive linear association was found between the coefficient of inbreeding and the magnitude of leaf damage, whereas a negative association was found between coefficient of inbreeding and several male and female fitness traits. When pesticides were used to control beetle herbivory, the interaction between coefficient of inbreeding and pesticide treatment was significant for fruit production and marginally significant for pollen quantity per anther. Therefore, the magnitude of inbreeding depression in C. pepo ssp. texana varies depending on the severity of beetle herbivory.
Cucumber beetles, Acalymma vittatum (F.) and Diabrotica undecipunctata howardi (Barber), are specialist herbivores of cucurbits and the vector of Erwinia tracheiphila (E.F. Smith) Holland, the causative agent of wilt disease. Cucumber beetles transmit E. tracheiphila when infected frass falls onto leaf wounds at the site of beetle feeding. We show that E. tracheiphila also can be transmitted via the floral nectaries of Cucurbita pepo ssp. texana L. Andres (Texas gourd). Under field conditions, we found that beetles aggregate in flowers in the late morning, that these beetles chew the anther filaments that cover the nectaries in male flowers thereby exposing the nectary, and that beetle frass accumulates on the nectary. We use real-time polymerase chain reaction to show that most of the flowers produced during the late summer possess beetle frass containing E. tracheiphila. Greenhouse experiments, in which cultures of E. tracheiphila are deposited onto floral nectaries, show that Texas gourds can contract wilt disease through the floral nectaries. Finally, we use green fluorescent protein-transformed E. tracheiphila to document the movement of E. tracheiphila through the nectary into the xylem of the pedicel before the abscission of the flower. Together, these data show that E. tracheiphila can be transmitted through infected frass that falls on or near the floral nectaries. We hypothesize that the concentration of frass from many beetles in the flowers increases both exposure to and the concentration of E. tracheiphila and plays a major role in the dynamics of wilt disease in both wild populations and cultivated squash fields.
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