Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae)

The landmark discovery of obligate pollination mutualism between Glochidion plants and Epicephala moths has sparked increased interest in the pollination systems of Phyllantheae plants. In this paper I review current information on the natural history and evolutionary history of obligate pollination mutualism in Phyllantheae. Currently, an estimated >500 species are mutualistic with Epicephala moths that actively pollinate flowers and whose progeny feed on the resulting seeds. The Phyllantheae also includes species that are not mutualistic with Epicephala moths and are instead pollinated by bees and/or flies or ants. Phylogenetic analyses indicate that the mutualism evolved independently five times within Phyllantheae, whereas active pollination behavior, a key innovation in this mutualism, evolved once in Epicephala . Reversal of mutualism has occurred at least once in both partner lineages, involving a Breynia species that evolved an alternative pollination system and a derived clade of Epicephala that colonized ant-pollinated Phyllantheae hosts and thereby lost the pollinating habit. The plant–moth association is highly species specific, although a strict one-to-one assumption is not perfectly met. A comparison of plant and moth phylogenies suggests signs of parallel speciation, but partner switches have occurred repeatedly at a range of taxonomic levels. Overall, the remarkable species diversity and multiple originations of the mutualism provide excellent opportunities to address many important questions on mutualism and the coevolutionary process. Although research on the biology of the mutualism is still in its infancy, the Phyllantheae– Epicephala association holds promise as a new model system in ecology and evolutionary biology.     

Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae)

About half a dozen obligate pollination mutualisms between plants and their seed-consuming pollinators are currently recognized, including fig-fig wasp, yucca-yucca moth, and the recently discovered Glochidion tree-Epicephala moth mutualisms. A common principle among these interactions is that the pollinators consume only a limited amount of the seed crop within a developing fruit (or fig in the case of fig-fig wasp mutualism), thereby ensuring a net benefit to plant reproduction. A novel obligate, seed-parasitic pollination mutualism between two species of New Caledonian Phyllanthus (Euphorbiaceae), a close relative of Glochidion, and Epicephala moths (Gracillariidae) is an exception to this principle. The highly specialized flowers of Phyllanthus are actively and exclusively pollinated by species-specific Epicephala moths, whose larvae consume all six ovules of the developing fruit. Some flowers pollinated by the moths remain untouched, and thus a fraction of the fruits is left intact. Additional evidence for a similar association of Epicephala moths in other Phyllanthus species suggests that this interaction is a coevolved, species-specific pollination mutualism. Implications for the evolutionary stability of the system, as well as differences in mode of interaction with respect to the Glochidion-Epicephala mutualism, are discussed.     

Obligate pollination mutualism in Breynia (Phyllanthaceae): further documentation of pollination mutualism involving Epicephala moths (Gracillariidae)

This paper reports obligate seed-parasitic pollination mutualisms in Breynia vitis-idea and B. fruticosa (Phyllanthaceae). The genus Breynia is closely related to Glochidion and Gomphidium (a subgenus of Phyllanthus), in which pollination by species-specific, seed-parasitic Epicephala moths (Gracillariidae) have been previously reported. At night, female Epicephala moths carrying numerous pollen grains on their proboscises visited female flowers of B. vitis-idea, actively pollinated flowers, and each subsequently laid an egg. Examination of field-collected flowers indicated that pollinated flowers of B. vitis-idea and B. fruticosa almost invariably had Epicephala eggs, suggesting that these moths are the primary pollinators of the two species. Single Epicephala larvae consumed a fraction of seeds within developing fruit in B. vitis-idea and all seeds in B. fruticosa. However, some of the fruits were left untouched, and many of these had indication of moth oviposition, suggesting that egg/larval mortality of Epicephala moths is an important factor assuring seed set in these plants. The overall similarity of the specialized floral structure among Breynia species may indicate that this pollination system is fairly widespread within the genus.     

Assessment of the diversity and species specificity of the mutualistic association between Epicephala moths and Glochidion trees

The obligate mutualisms between flowering plants and their seed-parasitic pollinators constitute fascinating examples of interspecific mutualisms, which are often characterized by high levels of species diversity and reciprocal species specificity. The diversification in these mutualisms has been thought to occur through simultaneous speciation of the partners, mediated by tight reciprocal adaptation; however, recent studies cast doubt over this general view. In this study, we examine the diversity and species specificity of Epicephala moths (Gracillariidae) that pollinate Glochidion trees (Phyllanthaceae), using analysis of mitochondrial and nuclear gene sequences. Phylogenetic analysis of Epicephala moths associated with five Glochidion species in Japan and Taiwan reveal six genetically isolated species that are also distinguishable by male genital morphology: (i) two species specific to single host species (G. acuminatum and G. zeylanicum, respectively); (ii) two species that coexist on G. lanceolatum; and (iii) two species that share two, closely-related parapatric hosts (G. obovatum and G. rubrum). Statistical analysis shows that the two species associated with G. lanceolatum are not sister species, indicating the colonization of novel Glochidion host in at least one lineage. Behavioural observations suggest that all six species possess the actively-pollinating habit, thus none of the studied species has become a nonmutualistic 'cheater' that exploits the benefit resulting from pollination by other species. Our results parallel recent findings in ecologically similar associations, namely the fig-fig wasp and yucca-yucca moth mutualisms, and contribute to a more general understanding of the factors that determine ecological and evolutionary outcomes in these mutualisms.     

Repeated colonization of remote islands by specialized mutualists

Mutualisms are ubiquitous in nature, but constraints imposed by specialization may limit their ability to colonize novel environments synchronously. The ability of mutualisms to reassemble following disturbance is central to understanding their response to global change. Here, we demonstrate that a highly specialized pollination mutualism considered to be obligate (Phyllanthaceae: Glochidion; Lepidoptera: Gracillariidae: Epicephala) has colonized some of the world's most isolated archipelagoes, and we record, to our knowledge, for the first time the presence of Epicephala moths from 19 host Glochidion species on 17 islands in the Pacific Ocean. Our findings appear to offer a remarkable example of mutualism persistence in an insect-plant interaction characterized by reciprocal specialization and mutual dependence. These findings also appear to contradict the island biogeography paradigm that taxa with specialized biotic interactions are unlikely to colonize oceanic islands.     

COSPECIATION ANALYSIS OF AN OBLIGATE POLLINATION MUTUALISM: HAVEGLOCHIDION TREES (EUPHORBIACEAE) AND POLLINATING EPICEPHALA MOTHS(GRACILLARIIDAE) DIVERSIFIED IN PARALLEL?

Species-specific obligate pollination mutualism between Glochidion trees (Euphorbiaceae) and Epicephala moths (Gracillariidae) involves a large number of interacting species and resembles the classically known fig-fig wasp and yucca-yucca moth associations. To assess the extent of parallel cladogenesis in Glochidion-Epicephala association, we reconstruct phylogenetic relationships of 18 species of Glochidion using nuclear ribosomal DNA sequences (internal and external transcribed spacers) and those of the corresponding 18 Epicephala species using mitochondrial (the cytochrome oxidase subunit I gene) and nuclear DNA sequences (the arginine kinase and elongation factor-1alpha genes). Based on the obtained phylogenies, we determine whether Glochidion and Epicephala have undergone parallel diversification using several different methods for investigating the level of cospeciation between phylogenies. These tests indicate that there is generally a greater degree of correlation between Glochidion and Epicephala phylogenies than expected in a random association, but the results are sensitive to selection of different phylogenetic hypotheses and analytical methods for evaluating cospeciation. Perfect congruence between phylogenies is not found in this association, which likely resulted from host shift by the moths. The observed significant discrepancy between Glochidion and Epicephala phylogenies implies that the one-to-one specificity between the plants and moths has been maintained through a complex speciation process or that there is an underestimated diversity of association between Glochidion trees and Epicephala moths.     

How to become a yucca moth: minimal trait evolution needed to establish the obligate pollination mutualism

The origins of obligate pollination mutualisms, such as the classic yucca–yucca moth association, appear to require extensive trait evolution and specialization. To understand the extent to which traits truly evolved as part of establishing the mutualistic relationship, rather than being pre‐adaptations, we used an expanded phylogenetic estimate with improved sampling of deeply‐diverged groups to perform the first formal reconstruction of trait evolution in pollinating yucca moths and their nonpollinating relatives. Our analysis demonstrates that key life‐history traits of yucca moths, including larval feeding in the floral ovary and the associated specialized cutting ovipositor, as well as colonization of woody monocots in xeric habitats, may have been established before the obligate mutualism with yuccas. Given these pre‐existing traits, novel traits in the mutualist moths are limited to the active pollination behaviours and the tentacular appendages that facilitate pollen collection and deposition. These results suggest that a highly specialized obligate mutualism was built on the foundation of pre‐existing interactions between early Prodoxidae and their host plants, and arose with minimal trait evolution. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 847–855.     

Reversal of mutualism in a leafflower–leafflower moth association: the possible driving role of a third‐party partner

A major goal in the study of mutualism is to understand how co‐operation is maintained when mutualism may potentially turn into parasitism. Although certain mechanisms facilitate the persistence of mutualism, parasitic species have repeatedly evolved from mutualistic ancestors. However, documented examples of mutualism reversals are still rare. Leafflowers (Phyllantheae; Phyllanthaceae) include approximately 500 species that engage in obligate mutualism with leafflower moths (Epicephala; Gracillariidae), which actively pollinate flowers, and whose larvae feed on the resulting seeds. We found that the Taiwanese population of the Phyllanthus reticulatus species complex was associated with six sympatric Epicephala species, of which three were derived parasites that induced gall formation on flowers/buds and produced no seeds. Notably, two parasitic species have retained mutualistic pollination behaviour, suggesting that the parasitism was likely not selected for to reduce the cost of mutualism. We propose that the galling habit evolved as an adaptation to escape parasitism by a specialized braconid wasp. The tough gall produced by one species was almost free of braconid parasitism, and the swollen gall induced by the other species probably prevents attack as a result of the larger airspace inside the gall. Our findings suggest that the presence of a third‐party partner can greatly influence the evolutionary fate of mutualisms, regardless of whether the pairwise interaction continues to favour co‐operation.     

传粉细蛾与大戟科植物专性授粉的互惠共生体系

在已知的昆虫与植物所形成的专性授粉互惠共生体系中,榕树—榕小蜂、丝兰—丝兰蛾体系是经典实例,国内外学者已经从不同角度进行了大量的研究,为我们理解植物—传粉者互惠共生体系协同进化的机理和历史积累了宝贵的资料。近些年的研究发现鳞翅目细蛾科头细蛾属昆虫与大戟科植物之间也存在相似的协同进化关系。文章对国内外学者有关传粉细蛾与大戟科植物互惠共生协同进化的研究进行了整理。     

Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

Brood pollination mutualisms—interactions in which specialized insects are both the pollinators (as adults) and seed predators (as larvae) of their host plants—have been influential study systems for coevolutionary biology. These mutualisms include those between figs and fig wasps, yuccas and yucca moths, leafflowers and leafflower moths, globeflowers and globeflower flies, Silene plants and Hadena and Perizoma moths, saxifrages and Greya moths, and senita cacti and senita moths. The high reciprocal diversity and species‐specificity of some of these mutualisms have been cited as evidence that coevolution between plants and pollinators drives their mutual diversification. However, the mechanisms by which these mutualisms diversify have received less attention. In this paper, we review key hypotheses about how these mutualisms diversify and what role coevolution between plants and pollinators may play in this process. We find that most species‐rich brood pollination mutualisms show significant phylogenetic congruence at high taxonomic scales, but there is limited evidence for the processes of both cospeciation and duplication, and there are no unambiguous examples known of strict‐sense contemporaneous cospeciation. Allopatric speciation appears important across multiple systems, particularly in the insects. Host‐shifts appear to be common, and widespread host‐shifts by pollinators may displace other pollinator lineages. There is relatively little evidence for a “coevolution through cospeciation” model or that coevolution promotes speciation in these systems. Although we have made great progress in understanding the mechanisms by which brood pollination mutualisms diversify, many opportunities remain to use these intriguing symbioses to understand the role of biotic interactions in generating biological diversity.     

A non‐pollinating moth inflicts higher seed predation than two co‐pollinators in an obligate pollination mutualism

1. Mutualisms are relationships of mutual exploitation, in which interacting species receive a net benefit from their association. In obligate pollination mutualisms (OPMs), female pollinators move pollen between the flowers of a single plant species and oviposit eggs within the female flowers that they visit. 2. Competition between co‐occurring pollinator species is predicted to increase pollinator virulence, i.e. laying more eggs or consuming more seeds per fruit. Plants involved in OPMs frequently host various non‐pollinating seed parasites and parasitoids that may influence the outcome of the mutualism. Quantifying the prevalence of parasites and parasitoids and competition between pollinators is important for understanding the factors that influence OPM evolutionary stability. 3. This study investigated the pollination mutualism occurring between the leaf flower plant, Breynia oblongifolia, and its co‐pollinating Epicephala moths. A third moth, Herpystis, also occurs in B. oblongifolia fruits as a non‐pollinating seed parasite. 4. Breynia oblongifolia fruits were collected to quantify seed predation and compare seed predation costs between the three moth species. Results showed that the larvae of the two pollinator species consume similar numbers of seeds, and that adults deposit similar numbers of eggs per flower. As such, no evidence of increases in virulent behaviours was detected as a result of competition between co‐pollinators. 5. By contrast, the seed parasite Herpystis consumed more seeds than either pollinator species, and fruit crops with a high proportion of Herpystis had significantly lower net seed production. 6. This work adds to the growing understanding of the ecology and dynamics of plant–pollinator mutualisms.     

Diffuse Coevolution between Two Epicephala Species (Gracillariidae) and Two Breynia Species (Phyllanthaceae)

The diffuse coevolution between two moth species (Epicephala lativalvaris and E. mirivalvata) and two plant species (Breynia fruticosa and B. rostrata) is reported based on field observations and indoor experiments conducted in Hainan and Fujian, China. Study results showed that the two Epicephala species jointly pollinated the two Breynia species, which led to a unique obligate pollination mutualism of two-to-two species specificity. A single Epicephala larva exclusively fed on seeds of host plants and developed to maturity by consuming all six seeds of each fruit, whereas a fraction of intact fruits were left to ensure the reproduction of plants within the whole population. Larvae of the two Epicephala species are competitive for resources; the population of E. mirivalvata is much smaller than that of E. lativalvaris, which has resulted from the differences in the female ovipositor structures and oviposition mode. The life history of Epicephala species highly coincides with the phenology of Breynia plants, and different phenology of B. fruticosa resulted in the different life history of the two Epicephala species in Hainan and Fujian. The natural hybridization of two host plants, possibly induced by the alternate pollination of two Epicephala species, is briefly discussed.     

中国头细蛾属昆虫(鳞翅目,细蛾科)与大戟科植物互利共生关系研究进展

细蛾科头细蛾属昆虫与大戟科算盘子属、叶下珠属和黑面神属植物互利共生关系的发现为研究昆虫与植物协同演化过程提供了一个全新的模式。目前,国内对头细蛾与大戟科植物的互利共生关系了解和研究都很少。本文介绍了头细蛾的分类、生物学和形态适应;大戟科相关5属植物(算盘子属、叶下珠属、黑面神属、白饭树属和守宫木属)的生物地理学,开花生物学,花的结构与传粉系统的关系;寄主植物与传粉者的对应关系;互利共生关系的维持机制等。研究表明中国有丰富的头细蛾与大戟科植物资源,开展其互利共生关系的研究有重要科学意义。很多新的、复杂的头细蛾与大戟科植物的生态关系和大量的头细蛾种类有待我们去发现和研究。     

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.     

Pollinator attraction to volatiles from virgin and pollinated host flowers in a yucca/moth obligate mutualism

The classic obligate pollination–seed consumption mutualism between yuccas and yucca moths has been thought to be mediated by chemical cues, but empirical data on pollinator attraction to host floral volatiles in this association have been lacking. Here we show that the scent from virgin flowers of the host Yucca glauca is sufficient to attract its obligate pollinator Tegeticula yuccasella in Y‐tube olfactometer tests. Interestingly, both sexes of moths were attracted to the scent stimulus. Because yucca moths mate inside host flowers, the attraction of both females and males to host floral volatiles is likely to increase encounter rates. In a second test, female moths did not discriminate between virgin and hand‐pollinated flowers, indicating no post‐pollination change in scent production by the host that would lead to a reduction in pollinator attraction and thereby limit exploitation of the available seeds in host flowers. However, other mechanisms that could stabilise the mutualism between T. yuccasella and its yucca hosts have already been documented, i.e. selective abortion of heavily infested flowers, and a female‐derived host‐marking pheromone. Headspace collection and GC–MS were used to identify the blend of floral volatiles emitted by Y. glauca, which was found to be very similar to those of two other allopatric capsular‐fruited species, Y. elata and Y. filamentosa, revealing strong conservation of this trait within Yucca section Chaenocarpa.     

Limiting the cost of mutualism: the defensive role of elongated gynophore in the leafflower–moth mutualism

Mutualisms are interactions from which both partners benefit but may collapse if mutualists’ costs and benefits are not aligned. Host sanctions are one mechanism whereby hosts selectively allocate resources to the more cooperative partners and thereby reduce the fitness of overexploiters; however, many mutualisms lack apparent means of host sanctions. In mutualisms between plants and pollinating seed parasites, such as those between leafflowers and leafflower moths, pollinators consume subsets of the seeds as larval food in return for their pollination service. Plants may select against overexploiters by selectively aborting flowers with a heavy egg load, but in many leafflower species, seeds are fully eaten in some fruits, suggesting that such a mechanism is not present in all species. Instead, the fruits of Breynia vitis-idaea have stalk-like structures (gynophore) through which early-instar moth larvae must bore to reach seeds. Examination of moth mortality in fruits with different gynophore lengths suggested that fruits with longer gynophore had higher moth mortality and, therefore, less seed damage. Most moth mortality occurred at the egg stage or as early larval instar before moths reached the seeds, consistent with the view that gynophore functions to prevent moth access to seeds. Gynophore length was unaffected by plant size, extent of moth oviposition, or geography; thus, it is most likely genetically controlled. Because gynophores do not elongate in related species whose pollinators oviposit directly into the ovary, the gynophore in B. vitis-idaea may have evolved as a defense to limit the cost of the mutualism.     

An interaction between a specialized seed predator moth and its dioecious host plant shifting from parasitism to mutualism

Seed predator/pollinator and host plant interactions, which may be considered as antagonistic, have the potential to provide good model systems for the study of the early stages of evolution towards mutualism. I describe a relationship between a seed predator, the geometrid moth Perizoma affinitatum , and the dioecious plant Silene dioica . The moth is an obligate seed predator on its host plant. The searching and ovipositing behaviour of the female moths, number of eggs deposited per flower, the pollinating ability of the moths and the seed consumption by the larvae are described as different parameters and studied in two Finnish coastal populations. A high pollinating ability and limited seed consumption by the predator was found and discussed in relation to fitness models of P. affinitatum and S. dioica . In a mutualistic relationship there must be a balance between the costs and benefits so that the seed production by the moths is larger than the seed consumption by the larvae, given a net seed output larger than zero. The data of the parameters included in a seed production/consumption model give a positive seed output when the proportion of S. dioica flowers pollinated by other non-predating insects is less than 60%. Accordingly, even if P. affinitatum would become the exclusive pollinator it would not endanger the survival of the host plant and both partners would benefit from this interaction. Limited seed consumption, high pollinating ability and host specificity as seen in the P. affinitatum and S. dioica interaction are considered to have been important pre-existing qualities in the evolution of the obligate mutualisms between yucca and yucca moths and fig and fig wasps. In isolated serpentine populations where the gene flow is restricted and co-pollinators are rare the interaction between P. affinitatum and S. dioica has the potential to shift from parasitism to mutualism.     

Mutualism favours higher host specificity than does antagonism in plant–herbivore interaction

Coevolved mutualisms often exhibit high levels of partner specificity. Obligate pollination mutualisms, such as the fig–fig wasp and yucca–yucca moth systems, represent remarkable examples of such highly species-specific associations; however, the evolutionary processes underlying these patterns are poorly understood. The prevailing hypothesis suggests that the high degree of specificity in pollinating seed parasites is the fortuitous result of specialization in their ancestors because these insects are derived from endophytic herbivores that are themselves highly host-specific. Conversely, we show that in the Glochidion–Epicephala obligate pollination mutualism, pollinators are more host-specific than are closely related endophytic leaf-feeding taxa, which co-occur with Epicephala on the same Glochidion hosts. This difference is probably not because of shifts in larval diet (i.e. from leaf- to seed-feeding), because seed-eating lepidopterans other than Epicephala do not show the same degree of host specificity as Epicephala. Species of a tentative sister group of Epicephala each attack several distantly related plants, suggesting that the evolution of strict host specificity is tied to the evolution of pollinator habit. These results suggest that mutualists can attain higher host specificity than that of their parasitic ancestors and that coevolutionary selection can be a strong promoter of extreme reciprocal specialization in mutualisms.     

宽瓣头细蛾形态及生物学特性研究

宽瓣头细蛾Epicephala lativalvaris Li, Wang & Zhang是最近发现在黑面神Breynia fruticosa和喙果黑面神B. rostrata上专性传粉的昆虫。通过野外观察宽瓣头细蛾的访花行为、 室内饲养宽瓣头细蛾幼虫及解剖黑面神和喙果黑面神果实, 首次对其个体发育过程中各虫态的形态特征及生活习性和生活史进行了详细研究。结果表明： 宽瓣头细蛾的生活史因气候的不同而出现差异, 其在福建厦门1年发生4~5代, 有4个羽化主要高峰期, 分别为5月上旬至中旬、 6月中旬至下旬、 8月及9月下旬至10月上旬, 11月中下旬有少数成虫羽化, 12月上旬至次年4月中旬以卵或蛹越冬; 而在海南鹦哥岭1年发生6代, 无越冬现象。成虫分别主动为黑面神或喙果黑面神传粉并将卵产于子房内, 幼虫以寄主植物种子为食, 需要消耗果实内全部6粒种子才能发育成熟, 但每个种群内留有20.37%~77.63%完好的果实, 以维持互利关系的稳定。两种植物的结实率近似, 但宽瓣头细蛾对喙果黑面神的果实危害率是黑面神的2.05倍。结果说明, 在宽瓣头细蛾 黑面神和喙果黑面神专性传粉互利共生关系中, 两种寄主植物所获得的利益近似, 但喙果黑面神为宽瓣头细蛾提供了更多的回报。研究结果为头细蛾属其他种类生物学特性的了解提供了借鉴, 并为探讨宽瓣头细蛾 黑面神和喙果黑面神专性传粉互利共生关系稳定性的维持机制提供了基本依据。     

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