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.     

Facultative non-mutualistic behaviour by an “Obligate” mutualist: “Cheating” by Yucca moths

The interaction between yucca moths (Tegeticula spp., Incurvariidae) and yuccas (Yucca spp., Agavaceae) is an obligate pollination/seed predation mutualism in which adult female yucca moths pollinate yuccas, and yucca moth larvae feed on yucca seeds. In this paper we document that individual yucca moths, which are capable of acting as mutualists, facultatively cheat by ovipositing in yucca pistils without attempting to transfer pollen. Additionally, a high proportion of flowers are unlikely to receive pollen even when pollination is attempted, because many yucca moths carry little or no pollen. The probability of occurrence of non-mutualistic behaviour is not affected by the amount of pollen a moth carries: moths with full pollen loads are just as likely to act non-mutualistically as moths carrying little or no pollen. We propose four hypotheses that could explain facultative non-mutualistic behaviour in yucca moths.Present address: Department of Biology, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada     

Geographic isolation trumps coevolution as a driver of yucca and yucca moth diversification

Coevolution is thought to be especially important in diversification of obligate mutualistic interactions such as the one between yuccas and pollinating yucca moths. We took a three-step approach to examine if plant and pollinator speciation events were likely driven by coevolution. First, we tested whether there has been co-speciation between yuccas and pollinator yucca moths in the genus Tegeticula (Prodoxidae). Second, we tested whether co-speciation also occurred between yuccas and commensalistic yucca moths in the genus Prodoxus (Prodoxidae) in which reciprocal evolutionary change is unlikely. Finally, we examined the current range distributions of yuccas in relationship to pollinator speciation events to determine if plant and moth speciation events likely occurred in sympatry or allopatry. Co-speciation analyses of yuccas with their coexisting Tegeticula pollinator and commensalistic Prodoxus lineages demonstrated phylogenetic congruence between both groups of moths and yuccas, even though moth lineages differ in the type of interaction with yuccas. Furthermore, Yucca species within a lineage occur primarily in allopatry rather than sympatry. We conclude that biogeographic factors are the overriding force in plant and pollinator moth speciation and significant phylogenetic congruence between the moth and plant lineages is likely due to shared biogeography rather than coevolution.     

Genetic consequences of specialization: yucca moth behavior and self-pollination in yuccas

Reciprocal specialization in interspecific interactions, such as plant-pollinator mutualisms, increases the probability that either party can have detrimental effects on the other without the interaction being dissolved. This should be particularly apparent in obligate mutualisms, such as those that exist between yucca and yucca moths. Female moths collect pollen from yucca flowers, oviposit into floral ovaries, and then pollinate those flowers. Yucca moths, which are the sole pollinators of yuccas, impose a cost in the form of seed consumption by the moth larvae. Here we ask whether there also is a genetic cost through selfish moth behavior that may lead to high levels of self fertilization in the yuccas. Historically, it has been assumed that females leave a plant immediately after collecting pollen, but few data are available. Observations of a member of the Tegeticula yuccasella complex on Yucca filamentosa revealed that females remained on the plant and oviposited in 66% of all instances after observed pollen collections, and 51% of all moths were observed to pollinate the same plant as well. Manual cross and self pollinations showed equal development and retention of fruits. Subsequent trials to assess inbreeding depression by measuring seed weight, germination date, growth rate, and plant mass at 5 months revealed significant negative effects on seed weight and germination frequency in selfed progeny arrays. Cumulative inbreeding depression was 0.475, i.e., fitness of selfed seeds was expected to be less than half that of outcrossed seeds. Single and multilocus estimates of outcrossing rates based on allozyme analyses of open-pollinated progeny arrays did not differ from 1.0. The discrepancy between high levels of behavioral self-pollination by the moths and nearly complete outcrossing in mature seeds can be explained through selective foreign pollen use by the females, or, more likely, pollen competition or selective abortion of self-pollinated flowers during early stages of fruit development. Thus, whenever the proportion of pollinated flowers exceeds the proportion that can be matured to ripe fruit based on resource availability, the potential detrimental genetic effects imposed through geitonogamous pollinations can be avoided in the plants. Because self-pollinated flowers have a lower probability of retention, selection should act on female moths to move among plants whenever moth density is high enough to trigger abortion. Received: 18 March 1996 \Accepted: 30 July 1996     

Re-evaluating the role of selective abscission in moth/yucca mutualisms

Conflicts of interest are common to mutualisms, particularly those derived from exploitative interactions. Conflicts of interest are particularly pronounced in pollination/seed predation mutualisms, such as moth/yucca interactions, where consumption of seeds by larvae of a plant's pollinator will raise the fitness of the pollinator but lower the fitness of the plant. A central question in these mutualisms is, therefore, “what limits seed predation?” If plants with excess flowers selectively abscise flowers containing many eggs, they may reduce seed predation and overall increase their fecundity. If eggs in abscised flowers die, selective abscission may additionally contribute to the limitation or regulation of pollinator populations, thereby decreasing the probability of future overexploitation. We examined the effect of selective abscission in the mutualism between Yucca kanabensis and one of its pollinating moths, Tegeticula altiplanella. Per capita mortality of moth eggs due to abscission was high (95.5%), but did not increase on inflorescences with more ovipositions per flower. Overall mortality was partitioned into two components based upon the proportion of visited flowers abscised (i.e. resource‐limitation) and additional mortality (=selective abscission). Resource‐limitation per se inflicted 93.9% egg mortality, or most of the mortality due to abscission. But, the average number of eggs in fruit was lower than the average number of eggs in flowers, indicating that there was some selectivity of abscission. However, neither source of mortality increased on inflorescences with more ovipositions per visited flower. Egg mortality resulting from selective abscission was not as high as possible, because the yuccas appeared to use oviposition‐damaged ovules as a cue for selective abscission, and there was considerable variation in the relationship between oviposition number and damaged ovules. However, even if yuccas had retained the flowers containing the fewest eggs, selective abscission still would not have been higher on inflorescences with more ovipositions per flower. Considering also that, 1) number of ovipositions is a poor predictor of the number of larvae that hatch and feed on the developing seeds in a fruit and that, 2) there are several moth/yucca interactions in which selective abscission does not occur, we conclude that abscission, and particular selective abscission, may have density‐limiting effects on moth populations, but will fail as general explanations for regulating the dynamics of moth populations.     

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.     

BREEDING STRUCTURE OF A YUCCA FILAMENTOSA (AGAVACEAE) POPULATION

Yucca filamentosa and its species-specific pollinator, the yucca moth, Tegeticula yuccasella (Lepidoptera: Prodoxidae), form a relationship that is often cited as a classic example of a coevolved plant-pollinator mutualism. Observations of the moth's behavior have led to predictions that moth dispersal is relatively limited and that, as a consequence, the self-compatible Y. filamentosa should experience relatively high rates of self-fertilization. In contrast, analyses of its mating system indicated that Y. filamentosa was predominantly outcrossed. To better understand effective breeding patterns in Y. filamentosa populations, 10 polymorphic allozyme loci were investigated to analyze the breeding structure of a natural Y. filamentosa population. Analyses revealed that Y. filamentosa is predominantly outcrossed, has multiply sired fruits, and that each fruit was sired by a different set of pollen donors. The effective number of pollen donors per fruit ranged from 1.56 to 3.13, indicating that some correlated mating exists within fruits. Paternity analyses revealed that pollen moved from 6 m to 293 m (mean = 118 m) within the study population and that a minimum of 10% of the progeny were sired by pollen originating outside of the population. These results are discussed in the context of the yucca–yucca moth mutualism.     

Interrelationships of yuccas and yucca moths

Purposeful pollination of yucca by females of a moth that produces larvae that feed on some of the seeds is a classic example of plant-animal mutualism. Recent research has focused on the complex interspecific nature of this association. Pollinators are members of two genera with different oviposition and larval biologies. There appear to be several sibling species among populations of the pollinator that were formerly considered to be a single widespread generalist, and these may include sympatric nonpollinator 'cheaters'. Bogus yucca moths, members of a third genus, which neither transport pollen nor feed in the seed but depend upon the inflorescences, are niche specific and often host-species specific and include one leaf-mining species. Their larvae can spend many years in diapause before synchronized development.     

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.     

Defection by plants in the yucca–yucca moth association: a test of the cheater plant hypothesis for Yucca treculeana

In mutualisms, an underlying conflict of interests may select for defection from providing benefits. In the obligate mutualism between yuccas and yucca moths, where pollination service and seeds for pollinator larvae are traded, it has been suggested that some individuals in a population of Y. baccata may defect by preventing pollinator egg or larvae from development. We tested this hypothesis in Y. treculeana , another species suggested to contain cheater plants. Five specific predictions were tested during two years of study. A prediction that a surplus of plants without pollinator larvae should be present was met. Predicted existence of two distinct fruit morphs was rejected, and none of several highly variable morphological traits were linked to presence/absence of larvae. Predicted excess of intact seeds in the fruits of plants without larvae was not found; in fact, such plants produced fewer seeds, contrary to the hypothesis. A suggestion that inverse frequency-dependent fitness could explain the pattern was rejected. Contrary to prediction, distribution of larvae of a closely related cheater yucca moth was positively associated with pollinator larvae, even though it would not be affected by the proposed killing mechanism. The results together provide strong support against the existence of cheater plants in Y. treculeana .     

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     

Limiting cheaters in mutualism: evidence from hybridization between mutualist and cheater yucca moths

Mutualisms are balanced antagonistic interactions where both species gain a net benefit. Because mutualisms generate resources, they can be exploited by individuals that reap the benefits of the interaction without paying any cost. The presence of such 'cheaters' may have important consequences, yet we are only beginning to understand how cheaters evolve from mutualists and how their evolution may be curtailed within mutualistic lineages. The yucca-yucca moth pollination mutualism is an excellent model in this context as there have been two origins of cheating from within the yucca moth lineage. We used nuclear and mitochondrial DNA markers to examine genetic structure in a moth population where a cheater species is parapatric with a resident pollinator. The results revealed extensive hybridization between pollinators and cheaters. Hybrids were genetically intermediate to parental populations, even though all individuals in this population had a pollinator phenotype. The results suggest that mutualisms can be stable in the face of introgression of cheater genes and that the ability of cheaters to invade a given mutualism may be more limited than previously appreciated.     

Oviposition and pollination behavior of the yucca moth,Tegeticula maculata (Lepidoptera: Prodoxidae), and its relation to the reproductive biology of Yucca whipplei (Agavaceae)

Summary The adult behavior of the yucca moth, Tegeticula maculata Riley, is finely tuned to the reproductive biology of its specific host plant, Yucca whipplei Torr. The female moths oviposit in the ovaries of the yucca flowers and actively pollinate the same flowers with pollen which they have collected previously. The selective pressures imposed on the moths by 1) the plant's need for pollen transfer via an insect pollinating agent, 2) its partial self-incompatibility, and 3) its ability to regulate seed set by aborting excess fruits, have molded the pollinator's behavior in such a way that its offspring have the greatest possible chance of surviving through the early larval stages. The evolutionary responses of the pollinator include the following: 1) the female moths consistently fly to a different plant after collecting pollen, thus insuring cross-fertilization of the flowers, 2) they always pollinate after depositing the first egg in a flower, but not necessarily after subsequent ovipositions, and 3) females emerging near the end of the flowering season frequently oviposit in developing seed pods, as opposed to open flowers which are more likely to be aborted by the plants.     

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.     

The role of abiotic and biotic factors in determining coexistence of multiple pollinators in the yucca–yucca moth mutualism

The determinants of a species' geographic distribution are a combination of both abiotic and biotic factors. Environmental niche modeling of climatic factors has been instrumental in documenting the role of abiotic factors in a species' niche. Integrating this approach with data from species interactions provides a means to assess the relative roles of abiotic and biotic components. Here, we examine whether the high host specificity typically exhibited in the active pollination mutualism between yuccas and yucca moths is the result of differences in climatic niche requirements that limit yucca moth distributions or the result of competition among mutualistic moths that would co‐occur on the same yucca species. We compared the species distribution models of two Tegeticula pollinator moths that use the geographically widespread plant Yucca filamentosa. Tegeticula yuccasella occurs throughout eastern North America whereas T. cassandra is restricted to the southeastern portion of the range, primarily occurring in Florida. Species distribution models demonstrate that T. cassandra is restricted climatically to the southeastern United States and T. yuccasella is predicted to be able to live across all of eastern North America. Data on moth abundances in Florida demonstrate that both moth species are present on Y. filamentosa; however, T. cassandra is numerically dominant. Taken together, the results suggest that moth geographic distributions are heavily influenced by climate, but competition among pollinating congeners will act to restrict populations of moth species that co‐occur.     

The influence of interaction type and feeding location on the phylogeographic structure of the yucca moth community associated with Hesperoyucca whipplei

The interactions between herbivorous insects and their host plants have been central in generating diversification in both groups. We used a community of four yucca moth species, monophagous on the host plant Hesperoyucca whipplei (Agavaceae), to examine how the type of interaction and where insects feed within a plant influence phylogeographic structure of herbivorous insects. These four species included two fruit-feeders, one mutualistic and one commensalistic, and two commensalistic stalk-feeders. Surveys based on mtDNA cytochrome oxidase I sequence data demonstrated that the moth species differed in phylogeographic history. Populations of the mutualist pollinator, Tegeticula maculata, exhibited the most subdivision in comparison to the three commensal Prodoxus species (both genera in Lepidoptera, Prodoxidae). Feeding location was also correlated with differences in phylogeographic history through its influence on population sizes and the probability of gene flow. The results suggest that both the outcome of interactions and where insects feed may influence population structure.     

Infertile seeds ofYucca schottii: A beneficial role for the plant in the yucca-yucca moth mutualism?

Summary The yucca-yucca moth interaction is a classic case of obligate mutualism. Female moths pollinate and oviposit in the gynoecium of the flower; however, maturing larvae eat a fraction of the developing seeds. We studied within-fruit distributions of four seed types (fertile, infertile, eaten and uneaten seeds) in order to evaluate costs and benefits in aYucca schottii population in southeastern Arizona. We focused on how the spatial arrangement of seeds affected larval behaviour and, hence, the costs of the mutualism to the yucca. Infertile seeds were distributed throughout both infested and uninfested locules. Additionally, moth larvae feeding in a single locule preferred fertile seeds and even avoided infertile seeds and left the fruit significantly more often when they encountered infertile seeds. We suggest that, regardless of the cause of infertile seeds, they function as blocking units within seed locules and therefore reduce seed predation by moth larvae. We also suggest that, together with certain other fruit traits, the presence of infertile seeds promotes the evolutionary stability of this pollination mutualism.     

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.     

The evolutionary ecology of cheating: does superficial oviposition facilitate the evolution of a cheater yucca moth?

Abstract 1. A major question in the study of mutualism is to understand how mutualists may revert to antagonists that exploit the mutualism (i.e. switch to cheating). In the classic pollination mutualism between yuccas and yucca moths, the cheater moth Tegeticula intermedia is sister to the pollinator moth T. cassandra. These moth species have similar ovipositor morphology, but T. intermedia emerges later, oviposits into fruit rather than flowers, and does not pollinate. 2. We tested if the pollinator, T. cassandra, was pre‐adapted to evolve a cheater lineage by comparing its emergence and oviposition behaviour on yucca fruit to a distantly related pollinator, T. yuccasella, that differs in ovipositor morphology and oviposition behaviour. We predicted that if T. cassandra was pre‐adapted to cheat, then these pollinators would emerge later and be able to oviposit into fruit in contrast to T. yuccasella. 3. Contrary to expectations, a common garden‐rearing experiment demonstrated that emergence of T. cassandra was not significantly delayed relative to T. yuccasella. Moth emergence patterns overlapped broadly. 4. No choice oviposition experiments with female moths demonstrated that both pollinator species attempted to oviposit into fruit, but only T. cassandra was successful. Four out of 84 T. cassandra successfully oviposited into older fruit, whereas zero out of 79 T. yuccasella oviposited into older fruit. The rarity of the cheating behaviour in pollinators, however, meant that no significant difference in oviposition ability was detected. 5. The results suggest that a shift in emergence phenology is likely not a pre‐adaptation to the evolution of cheating, but that the ability to successfully lay eggs into fruit may be. The results also demonstrate that cheating attempts are rare in these pollinator species and, hence, the evolutionary transition rate from pollinator to cheater is likely to be low.     

Regulation of moth–yucca mutualisms: mortality of eggs in oviposition-induced 'damage zones'

Pollination–seed predation mutualisms such as moth–yucca interactions are important model systems for studying mechanisms that limit exploitation when mutualistic partners have strong conflicts of interest. In many moth–yucca interactions, oviposition leads to the failure of some ovules to develop normally. Here, we demonstrate that moth eggs almost always perish if they are inside these oviposition‐induced ‘damage zones’ of developing fruit. Moreover, because more ovipositions result both in larger damage zones and in higher proportions of eggs within damage zones, this source of mortality is strongly density‐dependent. Therefore, mortality of eggs in oviposition‐induced damage zones may be an important process for limiting seed consumption and regulating moth densities in many moth–yucca mutualisms.