Costs of two non-mutualistic species in a yucca/yucca moth mutualism

Mutualisms often involve significant costs for participants. Costs are inflicted by mutualists themselves, as well as by associated, non-mutualistic species. These costs are rarely quantified, however, particularly the ones extrinsic to the pairwise interaction. We compare costs inflicted by an obligate mutualist pollinator and two common exploiters of an Arizona yucca over a 2-year period. The magnitude of seed damage from seed and fruit-feeding beetle larvae (Carpophilus longus, Nitidulidae) was similar to damage from the seed-eating larvae of Yucca schottii's pollinator moth Tegeticula yuccasella (Prodoxidae), averaging about 15 seeds destroyed per fruit in each case. The two seed predators usually fed within the same fruits, although rarely side by side. In contrast, the presence of fruit-galling moth larvae (Prodoxusy-inversus, Prodoxidae) appeared to benefit the yucca: individual Tegeticula destroyed only half as many seeds in galled fruits as they did in ungalled fruits. We discuss three general implications of these results. Firstly, the costs of non-mutualists to the two mutualistic partners are not necessarily parallel. Secondly, measurable costs of non-mutualists do not necessarily translate into an impact on the success of the mutualism itself, because they may be incurred after mutualistic activities take place. Finally, the costs of mutualists to each other can differ substantially depending on the presence or absence of non-mutualistic species. Received:17 July 1996 / Accepted:10 June 1997     

Variation in the costs and benefits of mutualism: the interaction between yuccas and yucca moths

Summary Yucca moths are both obligate pollinators and obligate seed predators of yuccas. I measured the costs and net benefits per fruit arising for eight species of yuccas from their interaction with the yucca moth Tegeticula yuccasella. Yucca moths decrease the production of viable seeds as a result of oviposition by adults and feeding by larvae. Oviposition through the ovary wall caused 2.3–28.6% of ovules per locule to fail to develop, leaving fruit with constrictions, and overall, 0.6–6.6% of ovules per fruit were lost to oviposition by yucca moths. Individual yucca moth larvae ate 18.0–43.6% of the ovules in a locule. However, because of the number of larvae per fruit and the proportion of viable seeds, yucca moth larvae consumed only 0.0–13.6% of potentially viable ovules per fruit. Given both oviposition and feeding effects, yucca moths decreased viable seed production by 0.6–19.5%. The ratio of costs to (gross) benefits varied from 0% to 30%, indicating that up to 30% of the benefits available to yuccas are subsequently lost to yucca moths. The costs are both lower and more variable than in a similar pollinator-seed predator mutualism involving figs and fig wasps.There were differences between species of yuccas in the costs of associating with yucca moths. Yuccas with baccate fruit experienced lower costs than species with capsular fruit. There were also differences in costs between populations within species and high variation in costs between fruit within populations. High variability was the result of no yucca moth larvae being present in over 50% of the fruit in some populations, while other fruit produced up to 24 larvae. I present hypotheses explaining both the absence and high numbers of larvae per fruit.     

Species identification and sibship assignment of sympatric larvae in the yucca moths Tegeticula synthetica and Tegeticula antithetica (Lepidoptera: Prodoxidae)

Ecological interactions between yucca moths (Tegeticula, Prodoxidae) and their host plants (Yucca, Agavaceae) are exemplary of obligate plant-pollinator mutualism and co-evolution. We describe a multiplex microsatellite DNA protocol for species identification and sibship assignment of sympatric larvae from Tegeticula synthetica and Tegeticula antithetica, pollinators of the Joshua tree (Yucca brevifolia). Bayesian clustering provides correct diagnosis of species in 100% of adult moths, with unambiguous identification of sympatric larvae. Sibship assignments show that larvae within a single fruit are more likely to be full-sibs or half-sibs than larvae from different fruit, consistent with the hypothesis that larval clutches are predominantly the progeny of an individual female.     

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.     

Inbreeding and outcrossing in Yucca whipplei: consequences for the reproductive success of plant and pollinator

Unlike most pollinators, yucca moths are active pollinators of their host plants. Females lay their eggs in the flowers they pollinate, and their larvae feed solely on the resulting seeds. Previous evidence suggests that the yucca moth Tegeticula maculata avoids self-pollinating their host Yucca whipplei . Other yucca moths may self-pollinate more frequently. When pollinating, yucca moths are also reported to fly large distances between plants, bypassing neighbouring plants in the process. We experimentally verify the suggestion of Pellmyr et al . that yucca is more likely to retain fruits from self-pollination if overall fruit set is low. Thus, selection on moths to avoid self-pollinating should be density dependent. We found no evidence that mating with close neighbours resulted in inbreeding depression, thus the moth's long-distance flights between plants are yet to be explained.     

Rapid evolution and specialization following host colonization in a yucca moth

Host shifts followed by specialization can result in sympatric genetic differentiation, and may have fuelled the diversification of phytophagous insects. This study examines a recent colonization of a non‐native host by Prodoxus quinquepunctellus (Lepidoptera: Prodoxidae). Allozyme differentiation was detected among different host feeding populations, yet was nearly absent among similar host feeding populations in sympatry. Geographical patterns of allozyme variation showed a much higher level of population structure among populations feeding on the derived host. Conversely, mtDNA haplotype frequencies were nearly homogeneous in the derived populations compared to the ancestral populations, suggesting a bottleneck and/or rapid fixation of haplotypes following host colonization. Moth emergence coincided with host plant flowering, and phenological differences between host species translated into allochronic isolation between populations feeding on different hosts. Derived moth populations also differed significantly in three ovipositor characters from ancestral populations. These findings suggest rapid host‐specific genetic differentiation, and specialization of moth emergence time and ovipositor morphology following host colonization.     

Synchronized,mass-emergences of a yucca moth,Prodoxus Y-inversus (Lepidoptera: Prodoxidae), after 16 and 17 years in diapause

Summary In 1985 and 1986, more than 180 adults of Prodoxus y-inversus Riley eclosed from cocoons of the 1969 generation in Yucca baccata, after prepupal larvae spent 16 and 17 years in diapause, intervals prior to mass emergence that are unmatched by any other insect on record. The emergences, which occurred during 15- to 16-day periods, followed many years of virtually no maturation by other individuals of the colony, and the size of the moths was not diminished by the long wait. Successful delay of development and synchronous emergence by many individuals indicates that whole populations can postpone activities through long periods of conditions that would be adverse for adult activity.     

Yucca moth oviposition and pollination behavior is affected by past flower visitors: evidence for a host-marking pheromone

Insect larvae such as those of yucca moths that feed on small, patchily distributed food items often face an elevated risk of intraspecific competition or cannibalism. For this reason, ovipositing females may assess a potential oviposition site for prior conspecific eggs or larvae before deciding whether to oviposit. Selective abortion of yucca flowers with high egg numbers prevents competition among larvae of the yucca moth Tegeticula yuccasella, but the same mechanism should select for female detection of and fewer ovipositions in flowers that already contain eggs. Female yucca moths presented with either virgin or previously visited flowers laid significantly fewer eggs in the latter flowers and pollinated them less often. A significant negative association was found between number of previous oviposition attempts in a flower and number of additional attempts by a female, suggesting a quantitative assessment of prior egg load, but the correlation coefficient was low. Factors contributing to this low correlation may include variation in signal quality, poor detection capability, uncertainty contributed by a variable oviposition attempt to egg ratio, and a variable response criterion based on recent female experience and physiological status. Females rationed their pollen by pollinating at decreasing frequency during a bout within a flower, and by depositing smaller pollen loads during later pollinations within a flower. Females ovipositing into a previously visited flower pollinated as frequently as would a first female for a given oviposition attempt within a flower, i.e., the probability of pollination after the nth oviposition was independent of whether it was performed by a first or a later moth. Experimental presentation of virgin flowers marked with a homogenate from female abdomens induced the same oviposition and pollination behavior as seen on previously visited flowers, suggesting the presence of a host-marking pheromone. Given that all eggs within a selectively aborted flower die, there may be selection among some yucca moths for providing a strong signal of floral egg status to conspecific females. Received: 1 December 1998 / Accepted: 7 February 1999     

Limiting the costs of mutalism: multiple modes of interaction between yuccas and yucca moths

In pollination–seed predation mutualisms between yuccas and yucca moths, conflicts of interest exist for yuccas, because benefits of increased pollination may be outweighed by increased seed consumption. These conflicts raise the problem of what limits seed consumption, and ultimately what limits or regulates moth populations. Although the current hypothesis is that yuccas should selectively abscise flowers with high numbers of yucca-moth eggs, within-inflorescence selective abscission occurs in only one of the three moth–yucca systems that we studied. It occurs only when oviposition directly damages developing ovules, and does not, therefore, provide a general explanation for the resolution of moth–yucca conflicts. Within-locule egg mortality provides an alternative and stronger mechanism for limiting seed damage, and generating density-dependent mortality for yucca-moth populations. However, the most important feature of moth–yucca systems is that they are diverse, encompassing multiple modes of interaction, each with different consequences for limiting and regulating yucca moths.     

Conflict of interest in a mutualism: documenting the elusive fig wasp-seed trade-off

The generally accepted view that mutualisms represent reciprocal exploitations implies a greater or lesser degree of inherent tension between the partners. This view emphasizes the importance of identifying conflicts of interest between the partners, and then attempting to quantify the effects of factors that influence costs and benefits to each. The natural history of the speciose fig-fig wasp pollination mutualisms permits such measurements. However, previous attempts to document the presumed tensions, which are expected to result in a negative relationship between the production of viable seeds and pollinator wasp offspring, have met with mixed results, casting doubt on the existence of the conflict. Here, we present hierarchical analyses of 929 fruits sampled from 30 crops representing nine species of monoecious New World figs. These analyses control for the confounding influences of variation in (1) pollination intensity (numbers of foundress pollinators); (2) flower number per fruit; and (3) the proportion of those flowers that develop, on seed and wasp production, both among and within crops. We thereby show that a negative relationship between the production of viable seeds and wasps is, in fact, ubiquitous, thus documenting this underlying tension inherent in the mutualism. We suggest that complex interactions of variables that influence costs and benefits are likely to be a general property of most mutualistic systems. <br>     

Regulation of the mutualism between yuccas and yucca moths: intrinsic and extrinsic factors affecting flower retention

Yuccas initiate far more flowers than they can mature as fruit, thereby providing opportunities for them to mature flowers of the highest quality. Flower quality in yuccas has both intrinsic and extrinsic components. Intrinsic components relate to flower morphology and inflorescence architecture. Yucca moths (Tegeticula spp., Incurvariidae), the sole pollinators and primary seed predators of most yuccas (Yucca spp., Agavaceae), mediate extrinsic components of flower quality through their ovipositions in flowers, and the quantity and quality of pollen that they transfer. In addition, intrinsic and extrinsic components interact as a function of flowering phenology and moth activity within inflorescences.
We investigated selective abscission of flowers in Y. kanabensis with respect to various combinations of intrinsic and extrinsic factors. First, we considered the effect of high and low pollen loads delivered to different subsets of flowers and in different presentation orders. In the absence of moth ovipositions, Y. kanabensis is sensitive to the amount of pollen that moths deliver and tends to retain high pollen flowers, even when all flowers receive sufficient pollen for full fertilization. However, pollen delivery sequence and the position of flowers with an inflorescence modify this high pollen effect. We then considered the interplay between high and low pollen combined with moth ovipositions and found that the number of ovipositions dominated the pollen effect. Finally, we considered number of ovipositions in conjunction with different flowers in the blooming sequence while controlling pollen levels and found that the clear effect of ovipositions on flower fate can be tempered by where the flower is in the blooming sequence.
These results have implications for the regulation of the mutualism between yuccas and yucca moths, indicating that yuccas are capable of regulating costs, retaining flowers of relative high quality and selectively abscising the rest. Yucca sensitivity to several intrinsic and extrinsic factors allows the plant to respond flexibly to the pollination environment and several species of moths.     

Pollination ecology of Yucca elata

The pollination biology of a population of 250 Yucca elata (Liliaceae) plants was studied in southern New Mexico. Yucca elata and the prodoxid yucca moth Tegeticula yuccasella have a mutualistic association that is essential for the successful sexual reproduction of both species. However, a wide range of other invertebrate species visit flowers during the day and at night. Our aim was to quantify the role of yucca moths and other invertebrate visitors in pollination and fruit set, using manipulative field experiments. Inflorescences were bagged during the day or night (N=12 inflorescences) to restrict flower visitors to either nocturnal or diurnal groups. Yucca moths were active exclusively nocturnally during the flowering period and thus did not visit inflorescences that were unbagged during the day. None of the 4022 flowers exposed only to diurnal visitors set fruit, whereas 4.6% of the 4974 flowers exposed only to nocturnal visitors (including yucca moths) produced mature fruit. The proportion of flowers producing fruit in the latter treatment was not significantly different from unbagged control inflorescences. In a series of experimental manipulations we also determined that: (1) flowers opened at dusk and were open for two days on average, but were only receptive to pollen on the first night of opening; (2) pollen must be pushed down the stigmatic tube to affect pollination; and (3) most plants require out-cross pollination to produce fruit. The combination of these results strongly suggests that yucca moths are the only species affecting pollination in Y. elata, and that if another species was to affect pollination, it would be a rare event.     

非传粉小蜂的食性及其对榕树-传粉小蜂系统稳定性的影响

榕树与其传粉小蜂形成了高度专一的互惠共生系统。非传粉小蜂则是该系统的资源掠夺者,但它与该系统共存的机制仍不清楚。于2003年12月-2004年4月在西双版纳以聚果榕（Ficus racemosa L．）为材料,研究了寄生在聚果榕榕果内的5种非传粉小蜂的食性及相互关系,以探讨非传粉小蜂与榕树-传粉小蜂系统共存的机制。结果表明：寄生在聚果榕榕果内的5种非传粉小蜂中,仅Platyneura testacea Motschulsky和Platyneura,mayri Rasplus能刺激子房发育成瘿花,是造瘿者;Apocrypta sp．,Apocrypta westwoodi Grandi和Platyneura agraensis Joseph不能刺激子房发育成瘿花,是拟寄生者。传粉小蜂的拟寄生者和造瘿者对传粉小蜂有负的影响。但在蚂蚁和造瘿者的拟寄生蜂作用下,这种负面影响并不显著,而且它们对榕树繁殖没有显著影响。对小蜂自然种群的分析表明,传粉小蜂处于优势地位。说明在自然情况下传粉小蜂的拟寄生者和造瘿者的种群维持在一个较低水平,对榕树一传粉小蜂系统稳定性影响较小,故能与之长期共存。     

Opportunism vs. specialization: the evolution of dispersal strategies in fleshy-fruited plants

Plant Ecology - In this paper we address two questions concerning the interaction between fleshy-fruited plants and their seed dispersers: (1) What determines optimal disperser coterie size...     

Examining genetic structure in a bogus yucca moth: a sequential approach to phylogeography

Understanding the phylogeography of a species requires not only elucidating patterns of genetic structure among populations, but also identifying the possible evolutionary events creating that structure. The use of a single phylogeographic test or analysis, however, usually provides a picture of genetic structure without revealing the possible underlying evolutionary causes. We used current analytical techniques in a sequential approach to examine genetic structure and its underlying causes in the bogus yucca moth Prodoxus decipiens (Lepidoptera: Prodoxidae). Both historical biogeography and recent human transplantations of the moth's host plants provided a priori expectations of the pattern of genetic structure and its underlying causes. We evaluated these expectations by using a progression of phylogenetic, demographic, and population genetic analyses of mtDNA sequence data from 476 individuals distributed across 25 populations that encompassed the range of P. decipiens. The combination of these analyses revealed that much of the genetic structure has evolved more recently than suggested by historical biogeography, has been influenced by changes in demography, and can be best explained by long distance dispersal and isolation by distance. We suggest that performing a suite of analyses that focus on different temporal scales may be an effective approach to investigating the patterns and causes of genetic structure within species.     

Critical population size for fig/wasp mutualism in a seasonal environment: effect and evolution of the duration of female receptivity

Fig trees and their pollinating wasps form ca. 750 pairs of obligate mutualists, mainly in the tropics. Survival of each partner depends on that of its associated species. Here, we examine the possible outcome of such an interaction at small population size. Using phenology data collected on Ficus natalensis in Gabon, we modelled wasp survival and the reproductive success of the trees according to the duration of receptivity of the tree, the amplitude of flowering seasonality, and the size of the fig tree population. Since the duration of receptivity is critical in these population level models, we also determined the influence of individual selection on this phenological trait. The models give three major results: (1) The minimum fig population size required to sustain a wasp population increases with the amplitude of seasonality, and decreases with increasing duration of receptivity; (2) tree population reproductive success is higher when the duration of receptivity is longer and when the population is large, but (3) individual selection toward a long duration of receptivity is weak or absent.     

The evolution of obligate pollination mutualisms: senita cactus and senita moth

We report a new obligate pollination mutualism involving the senita cactus, Lophocereus schottii (Cactaceae, Pachyceereae), and the senita moth, Upiga virescens (Pyralidae, Glaphyriinae) in the Sonoran Desert and discuss the evolution of specialized pollination mutualisms. L. schottii is a night-blooming, self-incompatible columnar cactus. Beginning at sunset, its flowers are visited by U. virescens females, which collect pollen on specialized abdominal scales, actively deposit pollen on flower stigmas, and oviposit a single egg on a flower petal. Larvae spend 6 days eating ovules before exiting the fruit and pupating in a cactus branch. Hand-pollination and pollinator exclusion experiments at our study site near Bahia Kino, Sonora, Mexico, revealed that fruit set in L. schottii is likely to be resource limited. About 50% of hand-outcrossed and open-pollinated senita flowers abort by day 6 after flower opening. Results of exclusion experiments indicated that senita moths accounted for 75% of open-pollinated fruit set in 1995 with two species of halictid bees accounting for the remaining fruit set. In 1996, flowers usually closed before sunrise, and senita moths accounted for at least 90% of open-pollinated fruit set. The net outcome of the senita/senita moth interaction is mutualistic, with senita larvae destroying about 30% of the seeds resulting from pollination by senita moths. Comparison of the senita system with the yucca/yucca moth mutualism reveals many similarities, including reduced nectar production, active pollination, and limited seed destruction. The independent evolution of many of the same features in the two systems suggests that a common pathway exists for the evolution of these highly specialized pollination mutualisms. Nocturnal flower opening, self-incompatible breeding systems, and resource-limited fruit production appear to be important during this evolution. Received: 19 August 1997 / Accepted: 24 November 1997