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Characterizing the interaction between the bogus yucca moth and yuccas: do bogus yucca moths impact yucca reproductive success?

Yucca moths are most well known for their obligate pollination mutualism with yuccas, where pollinator moths provide yuccas with pollen and, in exchange, the moth larvae feed on a subset of the developing yucca seeds. The pollinators, however, comprise only two of the three genera of yucca moths. Members of the third genus, Prodoxus, are the "bogus yucca moths" and are sister to the pollinator moths. Adult Prodoxus lack the specialized mouthparts used for pollination and the larvae feed on plant tissues other than seeds. Prodoxus larvae feed within the same plants as pollinator larvae and have the potential to influence yucca reproductive success directly by drawing resources away from flowers and fruit, or indirectly by modifying the costs of the mutualism with pollinators. We examined the interaction between the scape-feeding bogus yucca moth, Prodoxus decipiens, and one of its yucca hosts, Yucca filamentosa, by comparing female reproductive success of plants with and without moth larvae. We determined reproductive success by measuring a set of common reproductive traits such as flowering characteristics, seed set, and seed germination. In addition, we also quantified the percent total nitrogen in the seeds to determine whether the presence of larvae could potentially reduce seed quality. Flowering characteristics, seed set, and seed germination were not significantly different between plants with and without bogus yucca moth larvae. In contrast, the percent total nitrogen content of seeds was significantly lower in plants with P. decipiens larvae, and nitrogen content was negatively correlated with the number of larvae feeding within the inflorescence scape. Surveys of percent total nitrogen at three time periods during the flowering and fruiting of Y. filamentosa also showed that larval feeding decreased the amount of nitrogen in fruit tissue. Taken together, the results suggest that although P. decipiens influences nitrogen distribution in Y. filamentosa, this physiological effect does not appear to impact the female components of reproductive success.

Analysis of Variance↗

Resolving the "Yucca queretaroensis problem": Phylogenomic analysis of Yucca reveals the identity of an enigmatic species and the origin of an obligate pollination mutualism.

PREMISE: The genus Yucca is a group of ~50 species of woody monocots endemic to the North American arid regions. Their obligate pollination mutualism with yucca moths is considered a "textbook example" of coevolution and is hypothesized to have promoted rapid diversification. However, testing this hypothesis has been difficult due to uncertainty about the placement of a rogue taxon, Yucca queretaroensis, a rare endemic of the Sierra Gorda region of central Mexico. Past work placed this species in different positions within the Agavoideae, producing starkly different age estimates for Yucca (25 to 4 million years). METHODS: We generated new sequence capture data for 353 nuclear genes and for all coding regions of the plastid genome from wild-collected plants and samples included in previous studies to provide a new phylogeny and new age estimate for Yucca. RESULTS: The data presented here suggest that Y. queretaroensis is closely related to other species of Yucca. A relaxed molecular clock analysis of the plastid genome produced an estimated age for the genus of approximately 6.8 million years. CONCLUSIONS: The results resolve a mystery that has bedeviled evolutionary biologists for decades and provide a surprisingly young estimate for the age of Yucca, suggesting rapid diversification. The past difficulties in identifying the correct placement of Y. queretaroensis appear to be the product of laboratory errors, mistakes in field identification, and frequent hybridization with co-distributed taxa. The "Yucca queretaroensis problem" reaffirms the essential role for traditional botanical tools in phylogenomics.

ASTRAL↗

Multiple origins of the yucca-yucca moth association.

The association of species of yucca and their pollinating moths is considered one of the two classic cases of obligate mutualism between floral hosts and their pollinators. The system involves the active collection of pollen by females of two prodoxid moth genera and the subsequent purposeful placement of the pollen on conspecific stigmas of species of Yucca. Yuccas essentially depend on the moths for pollination and the moths require Yucca ovaries for oviposition. Because of the specificity involved, it has been assumed that the association arose once, although it has been suggested that within the prodoxid moths as a whole, pollinators have arisen from seed predators more than once. We show, by using phylogenies generated from three molecular data sets, that the supposed restriction of the yucca moths and their allies to the Agavaceae is an artifact caused by an incorrect circumscription of this family. In addition we provide evidence that Yucca is not monophyletic, leading to the conclusion that the modern Yucca-yucca moth relationship developed independently more than once by colonization of a new host.

Animals↗

Forty million years of mutualism: evidence for eocene origin of the yucca-yucca moth association.

The obligate mutualism between yuccas and yucca moths is a major model system for the study of coevolving species interactions. Exploration of the processes that have generated current diversity and associations within this mutualism requires robust phylogenies and timelines for both moths and yuccas. Here we establish a molecular clock for the moths based on mtDNA and use it to estimate the time of major life history events within the yucca moths. Colonization of yuccas had occurred by 41.5 +/- 9.8 million years ago (Mya), with rapid life history diversification and the emergence of pollinators within 0-6 My after yucca colonization. A subsequent burst of diversification 3.2 +/- 1.8 Mya coincided with evolution of arid habitats in western North America. Derived nonpollinating cheater yucca moths evolved 1.26 +/- 0.96 Mya. The estimated age of the moths far predates the host fossil record, but is consistent with suggested host age based on paleobotanical, climatological, biogeographical, and geological data, and a tentative estimation from an rbcL-based molecular clock for yuccas. The moth data are used to establish three alternative scenarios of how the moths and plants have coevolved. They yield specific predictions that can be tested once a robust plant phylogeny becomes available.

Animals↗

Phylogeographic structure in the bogus yucca moth Prodoxus quinquepunctellus (Prodoxidae): comparisons with coexisting pollinator yucca moths.

The pollination mutualism between yucca moths and yuccas highlights the potential importance of host plant specificity in insect diversification. Historically, one pollinator moth species, Tegeticula yuccasella, was believed to pollinate most yuccas. Recent phylogenetic studies have revealed that it is a complex of at least 13 distinct species, eight of which are specific to one yucca species. Moths in the closely related genus Prodoxus also specialize on yuccas, but they do not pollinate and their larvae feed on different plant parts. Previous research demonstrated that the geographically widespread Prodoxus quinquepunctellus can rapidly specialize to its host plants and may harbor hidden species diversity. We examined the phylogeographic structure of P. quinquepunctellus across its range to compare patterns of diversification with six coexisting pollinator yucca moth species. Morphometric and mtDNA cytochrome oxidase I sequence data indicated that P. quinquepunctellus as currently described contains two species. There was a deep division between moth populations in the eastern and the western United States, with limited sympatry in central Texas; these clades are considered separate species and are redescribed as P. decipiens and P. quinquepunctellus (sensu stricto), respectively. Sequence data also showed a lesser division within P. quinquepunctellus s.s. between the western populations on the Colorado Plateau and those elsewhere. The divergence among the three emerging lineages corresponded with major biogeographic provinces, whereas AMOVA indicated that host plant specialization has been relatively unimportant in diversification. In comparison, the six pollinator species comprise three lineages, one eastern and two western. A pollinator species endemic to the Colorado Plateau has evolved in both of the western lineages. The east-west division and the separate evolution of two Colorado Plateau pollinator species suggest that similar biogeographic factors have influenced diversification in both Tegeticula and Prodoxus. For the pollinators, however, each lineage has produced a monophagous species, a pattern not seen in P. quinquepunctellus.

Analysis of Variance↗

Effect of pollinator-inflicted ovule damage on floral abscission in the yucca-yucca moth mutualism: the role of mechanical and chemical factors.

The long-term persistence of obligate mutualisms (over 40 Mya in both fig/fig wasps and yucca/yucca moths) raises the question of how one species limits exploitation by the other species, even though there is selection pressure on individuals to maximize fitness. In the case of yuccas, moths serve as the plant's only pollinator, but eggs laid by the moths before pollination hatch into larvae that consume seeds. Previous studies have shown that flowers with high egg loads are more likely to abscise. This suggests that yucca flowers can select against moths that lay many eggs per flower through selective abscission of flowers; however, it is not known how yucca moths trigger floral abscission. We tested how the moth Tegeticula yuccasella triggers floral abscission during oviposition in Yucca filamentosa by examining the effects of ovipositor insertion and egg laying on ovule viability and floral abscission. Eggs are not laid at the site of ovipositor insertion: we used this separation to test whether wounded ovules were more closely associated with the ovipositor site or an egg's location. Using a tetrazolium stain to detect injured ovules, we determined whether the number of ovipositions affected the number of wounded ovules in naturally pollinated flowers. Two wounding experiments were used to test the effect of mechanical damage on the probability of floral abscission. The types of wounds in these experiments mimicked two types of oviposition-superficial oviposition in the ovary wall and oviposition into the locular cavity-that have been observed in species of Tegeticula. The effect of moth eggs on ovule viability was experimentally tested by culturing ovules in vitro, placing moth eggs on the ovules, and measuring changes in ovule viability with a tetrazolium stain. We found that ovules were physically wounded during natural oviposition. Ovules showed a visible wounding response in moth-pollinated flowers collected 7-12 h after oviposition. Exact location of wounded ovules relative to eggs and oviposition scars, as well as results from the artificial wounding experiments, showed that the moth ovipositor inflicts mechanical damage on the ovules. Significantly higher abscission rates were observed in artificially wounded flowers in which only 4-8% of the ovules were injured. Eggs did not affect ovule viability as measured by the tetrazolium stain. These results suggest that physical damage to ovules caused by ovipositing is sufficient to explain selective fruit abscission. Whether injury as a mechanism of selective abscission in yuccas is novel or a preadaptation will require further study.

Adaptation, Physiological↗

Testing the out-of-Florida hypothesis on the origin of cheating in the yucca-yucca moth mutualism.

Mutualistic interactions can be exploited by cheaters that take the rewards offered by mutualists without providing services in return. The evolution of cheater species from mutualist ancestors is thought to be possible under particular ecological conditions. Here we provide a test of the first explicit model of the transition from mutualism to antagonism. We used the obligate pollination mutualism between yuccas and yucca moths to examine the origins of a nonpollinating cheater moth, Tegeticula intermedia, and its pollinating sister species, T. cassandra. Based on geographic distribution and ecological factors affecting the pollinators, previous research had indicated that the cheaters evolved in Florida as a result of sympatry of T. cassandra and another pollinator species. We used mitochondrial DNA (mtDNA) sequences and amplified fragment length polymorphism (AFLP) data to investigate the phylogeographic history of the pollinator-cheater sister pair and to test whether the cheaters arose in Florida. Contrary to predictions, phylogenetic and population genetic analyses suggested that the cheaters evolved in the western United States and subsequently spread eastward. Western populations of cheaters had the most ancestral haplotypes and the highest genetic diversity, and there was also significant genetic structure associated with a geographic split between eastern and western populations. In comparison, there was evidence for weak genetic structure between northern and southern pollinator populations, suggesting a long history in Florida. The western origin of the cheaters indicated that the pollinators have more recently become restricted to the southeastern United States. This was supported by AFLP analyses that indicated that the pollinators were more closely related to the western cheaters than they were to geographically proximate cheaters in the east. Shared mtDNA between pollinators and eastern cheaters suggested hybridization, possibly in a secondary contact zone. The results negate the out-of-Florida hypothesis and reveal instead a long, complex, and disparate history for the pollinator-cheater sister pair.

Animals↗

Antiyeast steroidal saponins from Yucca schidigera (Mohave yucca), a new anti-food-deteriorating agent.

A saponin fraction from the stems of Yucca schidigera (Mohave yucca) exhibited potent growth-inhibitory activities against certain food-deteriorating yeasts, film-forming yeasts, and dermatophytic yeasts and fungi. From this fraction, a number of new anti-yeast monodesmosidic spirostanol saponins, named schidigera-saponins A1 (1), A2 (2), A3 (3), B1 (4), C1 (5),C2 (6); 25(R and S) schidigera-saponins D1 (7), D2 (8), E1 (12), F1 (13); and 25(S) schidigera-saponins D3 (9), D4 (10), D5 (11), and F2 (14) were isolated, together with several related known saponins, and the structures were elucidated by spectroscopic methods (see Chart 1). The relationship between the antiyeast activities and the structures of these saponins is described.

Animals↗

Occupational allergic contact urticaria to yucca (Yucca aloifolia), weeping fig (Ficus benjamina), and spathe flower (Spathiphyllum wallisii).

BACKGROUND: Occupational contact urticaria (CU) from plants is often reported, but it is less often attributed to decorative houseplants. We present an atopic gardener and caretaker of plants who developed CU when occupationally exposed to weeping fig, spathe flower, and yucca. METHODS: Sensitization was evaluated by skin prick tests (SPT) and analyses for IgE antibodies. RESULTS: SPT were positive to all three plants, and IgE antibodies were found to weeping fig and spathe flower. SPT were also performed with several decorative houseplants in more than 600 patients. Positive SPT was found to weeping fig (12%), African milk tree (8.3%), yucca (5.8%), Chinese rose (4.7%), massangana (4.6%), bird's nest fern (3.2%), and spathe flower (3.2%). CONCLUSION: Our study indicates that SPT and tests for IgE antibody are useful in detecting occupational CU caused by houseplants.

Adult↗

Studies on the use of Yucca schidigera to control giardiosis.

The potential anti-giardial activity of a powdered preparation of Yucca schidigera (yucca powder) was investigated in vitro, in a modified adherence inhibition assay, and in vivo, by enumeration of trophozoites (intestinal) or cysts (fecal) in experimentally infected gerbils and lambs receiving oral doses of whole or butanol-extracted yucca powder. Yucca powder, butanol-, acetone- and chloroform-extracted powder, and the butanol-insoluble fraction of the powder were required in concentrations of 22, 15, 62, 135 and 250 microg/ml, respectively, to reduce in vitro trophozoite adherence by 50%. Ethyl ether extract exhibited no anti-giardial activity. Virtually no trophozoites were tolerant of butanol extract at >or=90 microg/ml. Butanol extract at 1500 microg/ml exerted effects on trophozoites similar to the nitroimidazole, metronidazole, at 40 microg/ml during a 27-h incubation. Reducing trophozoite adherence to 50% of the controls required 5-10h of exposure to butanol extract or metronidazole. Oral administration of butanol extract (6.1mg) or metronidazole (1mg) once daily for 3 days reduced the number of trophozoites in the small intestine of infected gerbils, significantly (P<0.05) in the jejunum and ileum, and numerically (P>0.05) in the duodenum (n=8). Oral dosing of 50mg of butanol extract in eight doses over 3 days reduced (P<0.05) trophozoites in the duodenum and jejunum, and eliminated them from the ileum. Including 4.5% (w/w) yucca powder in the diet did not alter Giardia trophozoite recovery from the duodenum or jejunum of infected gerbils, but trophozoite reduction (P=0.051) was observed in the ileum (n=9). Jejunum gut loop data were inconclusive, possibly due to insufficient duration of exposure of trophozoites to butanol extract. Compared to controls (0g yucca powder per day) lambs receiving 10g of yucca powder per day in their diet shed fewer (P<0.05) Giardia cysts in their feces after 5, 9, 12 and 19 days of treatment, but a corresponding decline in the prevalence of infection was not observed (n=10). After 26 days, Giardia infections persisted in 90% of the lambs in both treatment groups. At the dosing levels studied in vivo, yucca powder did not affect the extent of cyst shedding by experimentally infected lambs, but further purification and concentration of the saponin fraction from Y. schidigera may provide the anti-giardial effects observed in vitro and in dosing trials.

Administration, Oral↗

Multiple occurrences of mutualism in the yucca moth lineage.

The complex mutualism between yuccas and the moths that pollinate their flowers is regarded as one of the most obvious cases of coevolution. Studies of related genera show that at least two of the critical behavioral and life history traits suggested to have resulted from coevolved mutualism in yucca moths are plesiomorphic to the family. Another trait, oviposition into flowers, has evolved repeatedly within the family. One species with these traits, Greya politella, feeds on and pollinates plants of a different family, but pollination occurs through a different component of the oviposition behavior than in the yucca moths. Major differences compared with yucca moths and their hosts are that G. politella only passively pollinates its host and that copollinators often contribute to pollination. This analysis suggests that evolution of mutualism between yuccas and yucca moths may have required few behavioral and life history changes in the moths. The truly coevolved features of this interaction appear to be the evolution of active pollination by the moths, the associated morphological structures in the moths for carrying pollen, and the exclusion of copollinators by yuccas.

Journal Article↗

Pollen dispersal in Yucca filamentosa (Agavaceae): the paradox of self-pollination behavior by Tegeticula yuccasella (Prodoxidae).

We investigated pollen dispersal in an obligate pollination mutualism between Yucca filamentosa and Tegeticula yuccasella. Yucca moths are the only documented pollinator of yuccas, and moth larvae feed solely on developing yucca seeds. The quality of pollination by a female moth affects larval survival because flowers receiving small amounts of pollen or self-pollen have a high abscission probability, and larvae die in abscised flowers. We tested the prediction that yucca moths primarily perform outcross pollinations by using fluorescent dye to track pollen dispersal in five populations of Y. filamentosa. Dye transfers within plants were common in all populations (mean ± 1 SE, 55 ± 3.0%), indicating that moths frequently deposit self-pollen. Distance of dye transfers ranged from 0 to 50 m, and the mean number of flowering plants between the pollen donor and recipient was 5 (median = 0), suggesting that most pollen was transferred among near neighbors. A multilocus genetic estimate of outcrossing based on seedlings matured from open-pollinated fruits at one site was 94 ± 6% (mean ± 1 SD). We discuss why moths frequently deposit self-pollen to the detriment of their offspring and compare the yucca-yucca moth interaction with other obligate pollinator mutualisms in which neither pollinator nor plant benefit from self-pollination.

Journal Article↗

Effect of different dietary levels of Yucca schidigera powder on the performance, blood parameters and egg yolk cholesterol of laying quails.

A total of 135 laying quails (Coturnix coturnix japonica), 9 weeks old, were divided into three dietary treatment groups. Three replicates were assigned to each treatment group consisting of 15 birds per cage. The diet was supplemented with 0, 100 and 200 ppm Yucca schidigera powder and given ad libitum to the quails for a period of 14 weeks. Body weight, egg production, feed consumption and feed efficiency were not different due to dietary treatments among the groups. Increased egg weight was determined in the control group. Yucca powder supplementation decreased serum glucose, cholesterol triglyceride level in laying quails. Serum total protein concentration was not changed by dietary treatments but albumin level was decreased in quails fed 100 ppm yucca powder. Egg yolk cholesterol concentration was not significantly different among the groups but tended to decline (11.5%) as a result of yucca supplementation. Red Blood Cell (RBC) and White Blood Cell (WBC) counts, packed cell volume (PCV), mean corpuscular volume (MCV) and mean corpuscular haemoglobin (MCH) were not affected by supplementation of yucca powder. However, haemoglobin (HB) concentration was slightly increased and mean corpuscular haemoglobin concentration (MCHC) was significantly increased by 200 ppm yucca powder supplementation to the diet.

Animal Feed↗

Strong conservation of floral scent composition in two allopatric yuccas.

Floral scent has been suggested to play a key role in the obligate pollination mutualism between yuccas and yucca moths. We analyzed floral fragrance compounds of Yucca elata with headspace collection followed by gas chromatography and mass spectrometry, and compared the odor blend with the recently characterized blend of the allopatric Yucca filamentosa. A principal component analysis based on 20 scent compounds revealed that the floral odor bouquets of Y. elata and Y. filamentosa are virtually identical. Although the two plants belong to the same section of capsular-fruited yuccas, they rely on different species of Tegeticula moths for pollination and probably have been allopatric for several million years. Yet, their floral odor blends are very similar, which may indicate that strong selection by obligate pollinators counteracts drift or divergence in this trait.

Animals↗

Ruminal metabolism in sheep of saponins from Yucca schidigera.

Fifty-five mg per kg live weight of crystallized Yucca schidigera saponins, corresponding to 26 mg/kg live weight of sapogenins, was given daily intraruminally to two lambs for 11 consecutive days. Neither of the lambs showed any sign of toxicity throughout the experimental period. One lamb was killed 5 h after the last dose and GC-MS analysis of the free and conjugated sapogenin content samples of liver, and of the contents of the rumen, omasum, abomasum, duodenum, jejunum, ileum, colon and rectum, of faecal samples collected before dosing started, and of parts of the administered Yucca saponin were performed. The Yucca material contained mainly sarsasapogenin and smilagenin saponins. Ingested saponins were quickly hydrolysed in the rumen to free sapogenins and, in part, epimerized at C-3 to afford episapogenins. The absorption of free sapogenins appeared to occur in the jejunum. The metabolism of Yucca saponins was identical to that of Narthecium ossifragum saponins, and it is suggested that Yucca saponins could replace N. ossifragum saponins for toxicity studies on the latter plant.

Animals↗

Investigation of spectrophotometrically determined substances in Yucca extract by GC/MS, TLC and on-column injection GC.

Spectrophotometrically determined substances in Yucca extract, listed as "Yucca foam extract" in the "List of Existing Food Additives in Japan", were investigated by GC/MS, TLC and GC. A TLC method using an anisaldehyde color developing reagent similar to that employed in spectrophotometry was established for selective detection of sapogenins in Yucca extract. Several steroidal sapogenins were found by GC/MS in the fractions corresponding to spots on the TLC plate, and these were assumed to have contributed to the color development in spectrophotometry. Sarsasapogenin and smilagenin were the dominant sapogenins. An on-column injection GC method to determine these sapogenins in Yucca extract was also developed. The sum of these two sapogenins in Yucca extract was 0.9%. The total amount of sapogenin estimated by GC was approximately 2%, which was similar to that measured by spectrophotometry.

Chromatography, Gas↗

Experimental and numerical simulation of dissolution and precipitation: implications for fracture sealing at Yucca Mountain, Nevada.

Plugging of flow paths caused by mineral precipitation in fractures above the potential repository at Yucca Mountain, Nevada could reduce the probability of water seeping into the repository. As part of an ongoing effort to evaluate thermal-hydrological-chemical (THC) effects on flow in fractured media, we performed a laboratory experiment and numerical simulations to investigate mineral dissolution and precipitation under anticipated temperature and pressure conditions in the repository. To replicate mineral dissolution by vapor condensate in fractured tuff, water was flowed through crushed Yucca Mountain tuff at 94 degrees C. The resulting steady-state fluid composition had a total dissolved solids content of about 140 mg/l; silica was the dominant dissolved constituent. A portion of the steady-state mineralized water was flowed into a vertically oriented planar fracture in a block of welded Topopah Spring Tuff that was maintained at 80 degrees C at the top and 130 degrees C at the bottom. The fracture began to seal with amorphous silica within 5 days.A 1-D plug-flow numerical model was used to simulate mineral dissolution, and a similar model was developed to simulate the flow of mineralized water through a planar fracture, where boiling conditions led to mineral precipitation. Predicted concentrations of the major dissolved constituents for the tuff dissolution were within a factor of 2 of the measured average steady-state compositions. The mineral precipitation simulations predicted the precipitation of amorphous silica at the base of the boiling front, leading to a greater than 50-fold decrease in fracture permeability in 5 days, consistent with the laboratory experiment.These results help validate the use of a numerical model to simulate THC processes at Yucca Mountain. The experiment and simulations indicated that boiling and concomitant precipitation of amorphous silica could cause significant reductions in fracture porosity and permeability on a local scale. However, differences in fluid flow rates and thermal gradients between the experimental setup and anticipated conditions at Yucca Mountain need to be factored into scaling the results of the dissolution/precipitation experiments and associated simulations to THC models for the potential Yucca Mountain repository.

Chemical Precipitation↗