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(American Journal of Botany. 2004;91:410-415.)
© 2004 Botanical Society of America, Inc.

Reproductive Biology

Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae)1

Atsushi Kawakita2 and Makoto Kato

Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo, Kyoto 606-8501, Japan

Received for publication July 17, 2003. Accepted for publication October 30, 2003.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
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.

Key Words: Epicephala • Gomphidium • New Caledonia • obligate pollination mutualism • Phyllanthus • stability of mutualism


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Obligate, seed-parasitic pollination mutualisms have arisen repeatedly during the history of terrestrial ecosystems. Currently recognized examples of such interactions involve plant and insect groups of various lineages (Janzen, 1979 ; Pellmyr, 1989 , 2003 ; Thompson and Pellmyr, 1992 ; Pellmyr et al., 1996 ; Fleming and Holland, 1998 ; Weiblen, 2002 ; Kato et al., 2003 ). These mutualisms range from highly coevolved (Janzen, 1979 ; Weiblen, 2002 ; Kato et al., 2003 ; Pellmyr, 2003 ) to less specialized interactions (Pellmyr, 1989 ; Thompson and Pellmyr, 1992 ; Pellmyr et al., 1996 ; Fleming and Holland, 1998 ), but the underlying principle is the same: pollination is accompanied by oviposition in flowers, and the larvae consume only a fraction of the seeds within a resulting fruit. In figs, there is only a single ovule per fruit, but the fig can be considered as an aggregate fruit containing many seeds, some of which are consumed by the pollinator larvae. The special case involves the functionally dioecious figs, in which the pollinator wasps occupy nearly all of the ovules within functionally male syconia (Galil, 1973 ; Janzen, 1979 ; Weiblen, 2002 ).

Given the described principle in most obligate pollination interactions, it has been assumed that excessive exploitation of seeds by pollinators would confer a substantial cost to plants and would subsequently lead to a collapse of the mutualistic relationship (Bull and Rice, 1991 ; Herre et al., 1999 ; Bronstein, 2001 ; Holland and DeAngelis, 2001 ). In this paper, we describe an obligate, seed-parasitic pollination mutualism in which a single larva of a pollinator moth consumes all seeds of the host fruit. This system, which involves New Caledonian Phyllanthus (subgenus Gomphidium) trees and gracillariid Epicephala moths, resembles the closely related Glochidion–Epicephala mutualism in terms of overall net outcome (Kato et al., 2003 ), but differs strikingly in the modes of interaction between the mutualists. These differences would allow for explicit comparative analyses on various aspects of interspecific mutualism and make these associations an important model system for general studies of coevolution.

Phyllanthus is a cosmopolitan genus of monoecious trees or herbs comprising more than 800 species (Govaerts et al., 2000 ). Although regarded as a nonmonophyletic group (Webster, 1994 ), it is the third largest genus of the family Euphorbiaceae (Govaerts et al., 2000 ). Among the 10 subgenera currently recognized, Gomphidium is a group of small trees comprising about 150 species restricted to Australia, New Guinea, and Polynesia (Holm-Nielsen, 1979 ). Notably, this subgenus has undergone extensive diversification in New Caledonia (115 species) and now constitutes the largest genus on the islands (Schmid, 1991 ). Most trees in this genus have a narrow distribution and use diverse habitats, ranging from rainforests to dry sclerophyllus scrubs, from calcareous to serpentinous soils, and from mangroves to high mountains. In New Caledonia, the subgenus is further divided into two sections, Gomphidium and Adenoglochidion; the former is distinguished from the latter by folded calyx lobes in the male flowers (Fig. 1). Our analyses reveal that at least one species representing each section is actively and exclusively pollinated by host-specific seed-parasitic moths. Additional evidence of moth associations in other species and the overall similarity of the highly specialized flowers within the group further suggest that this mutualism can potentially be generalized to most, if not all, species of the subgenus Gomphidium.



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  		Fig. 1. Flowers of Phyllanthus bourgeoisii (A–C) and P. aeneus (D–F). (A) Male flower. (B) Female flower. (C) Longitudinal section of a female flower. The arrow indicates the location of an Epicephala moth egg. (D) Male flower. (E, F) Female flowers. Epicephala eggs are laid within the tissue of the calyx lobes (arrow)

 

   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
We studied the pollination biology of 25 Phyllanthus species at various localities in New Caledonia during 29–31 August 2001, 7–13 September 2001, 19–29 March 2002, and 29 October–8 November 2002. Insect flower visitors were observed for two Phyllanthus species: P. bourgeoisii at Chutes de Ba (21°3' S, 164°7' E) during 31 October–2 November 2002 and P. aeneus at Cap Bocage (21°2' S, 164°6' E) during 27–29 March 2002. Phyllanthus bourgeoisii is a common rheophyte on rocky riverbanks, and P. aeneus is a shrub that is typical of serpentine scrub habitats (Figs. 2, 3). Phyllanthus aeneus has open male flowers, whereas those of P. bourgeoisii have folded calyx lobes, which make the anthers inaccessible to facultative flower visitors (Fig. 1). Female flowers of both species are much reduced and consist of short, fused styles that are mostly covered with calyx lobes (Fig. 1). The flowers have three locules, each containing two ovules. The two species flowered and fruited throughout the period of our study, which suggests an extended duration of flower and fruit production that is typical in Glochidion and other closely related genera (A. Kawakita and M. Kato, unpublished data).



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  		Figs. 2–9. Flowers and pollinators of Phyllanthus bourgeoisii and P. aeneus. 2. Overview of P. bourgeoisii. 3. Overview of P. aeneus. 4. Female Epicephala moth collecting pollen from a male flower of P. bourgeoisii. 5. Female Epicephala moth ovipositing in a female flower of P. aeneus. 6. Lateral view of a female Epicephala moth collected on P. aeneus showing its pollen-coated proboscis. Scale bar = 1 mm. 7. Scanning electron micrograph of a female Epicephala moth collected on P. bourgeoisii. The proboscis is dusted with pollen grains (indicated with an arrow). 8. Apical view of a P. bourgeoisii female flower. Pollen grains are deposited on the inner surface of the fused styles enclosed by the calyx lobes. Scale bar = 1 mm. 9. A P. aeneus fruit damaged by an Epicephala moth larva. The arrow indicates the exit hole

 
For each species, we spent a total of more than 30 h for diurnal and nocturnal observation of flower visitors. Particular effort was made so that our observations cover a wide range of the 24-h period. After field observations, we collected female flowers and mature fruits of the two species to assess the state of pollination and Epicephala moth oviposition and extent of seed infestation by the moth larvae. In the laboratory, we dissected the flowers using a light microscope and looked for the presence or absence of pollen grains on stigmas and Epicephala moth eggs in flowers. In the same way, we recorded the number of intact seeds within each mature fruit and assessed the cause of seed destruction for each fruit. Seed destruction was either caused by mature Epicephala larvae or by immature larvae that were parasitized by braconid wasps. For fruits from which moths/wasps had already emerged, we assessed the cause of seed destruction based on differences in exit-hole structure. In addition to the two species that we studied intensively, we also sampled female flowers of 10 Phyllanthus species and mature fruits of 23 species in order to infer the occurrence of moth oviposition in pollinated flowers and seed destruction by moth larvae in these plants. A list of species sampled and sample sizes of flowers and fruits examined is provided in Table 1.


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  		Table 1. A list of Phyllanthus species examined in the present study with information on locality and date of collection, presence/absence of Epicephala moths associated with fruits, and intensity of moth oviposition and fruit infestation. Intensity of fruit infestation for species with asterisks could not be determined due to degradation of the plant materials

 
To determine the extent to which the moths associated with different Phyllanthus hosts are genetically related, we analyzed nucleotide sequence variation within and among moth individuals reared from fruits of different Phyllanthus hosts: P. bourgeoisii (N = 7), P. aeneus (N = 5), P. chamaecerasus (N = 3), P. tiebaghiensis (N = 3), P. guillauminii (N = 5), and P. mangenotii (N = 2). Fruits used for rearing were collected from as many plant individuals as possible for each species in order to minimize the possibility that different moths shared the same mother (fruits were collected from the same plants used for examining seed infestation; see Table 1 for the number of individuals sampled). We extracted genomic DNA from ethanol-preserved larvae or adult moths reared from fruits of each species using the DNeasy Tissue Kit (Qiagen, Valencia, California, USA). For each individual moth, we amplified an approximately 1.4-kb fragment of the mitochondrial cytochrome oxidase subunit 1 gene (COI) using polymerase chain reaction (PCR) and primers described by Kato et al. (2003) . The PCR products were purified using a QIAquick PCR Purification Kit (Qiagen). The dye terminator cycle sequencing reaction was performed with an ABI PRISM Dye Terminator Cycle Sequencing Ready Reaction Kit (Perkin-Elmer, Foster City, California, USA) with the PCR primers and additional sequencing primers described by Kato et al. (2003) and electrophoresed on an ABI 3100 sequencer (Perkin-Elmer). Alignment of sequences was straightforward and required no gaps. Using PAUP* version 4.0b10 (Swofford, 2002 ), we calculated uncorrected pairwise distances within 1317 bp of the COI gene and estimated relative branch lengths using the neighbor-joining method. All sequences obtained in this study have been deposited in GenBank under accession numbers AY269392–AY269416.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
During our field observations, Epicephala moths were the only visitors to Phyllanthus flowers. In the evening, females of undescribed Epicephala species used their proboscises to collect pollen from male Phyllanthus flowers (Fig. 4). We observed four visits by Epicephala moths to male flowers of P. bourgeoisii and one visit to male flowers of P. aeneus. On separate occasions, we recorded two visits by female Epicephala moths to female flowers of P. bourgeoisii and two visits to those of P. aeneus. All of these moths deliberately deposited pollen on the stigma with their proboscises and subsequently laid an egg (Fig. 5). Flower-visiting females consistently carried numerous pollen grains on their proboscises (Figs. 6, 7), and their behavior on flowers was similar to that observed in Glochidion-pollinating Epicephala moths (Kato et al., 2003 ). The low number of observations reflects the extreme difficulty of encountering moth visits even during the peak flowering period, which was also the case in Glochidion-pollinating Epicephala (A. Kawakita and M. Kato, personal observations).

In both Phyllanthus species, pollen grains were deposited on the inner surface of the fused styles (Fig. 8), which likely did not occur through passive pollination. In P. bourgeoisii, moth eggs were laid into the narrow pit of the style apex (Fig. 1), whereas in P. aeneus, eggs were laid directly into the tissue of the calyx lobes (Fig. 1). Surprisingly, not all pollinated flowers contained eggs; of 81 pollinated female flowers of P. bourgeoisii, only 49% had eggs, while of 45 pollinated P. aeneus flowers, 69% contained eggs. Phyllanthus bourgeoisii flowers used for oviposition invariably had one egg per flower, whereas 25% and 8% of infested P. aeneus flowers contained two and three eggs, respectively. Unpollinated flowers did not contain moth eggs (N = 32 and 15 for P. bourgeoisii and P. aeneus, respectively).

Of 136 mature fruits of P. bourgeoisii, 28% were infested by Epicephala larvae, and of 42 mature P. aeneus fruits, 40% were attacked (Fig. 10). Each larva consumed all six ovules to complete larval growth and emerged from the fruit to pupate on the host leaves or in litter (Fig. 9). In P. bourgeoisii, 58% of Epicephala larvae were parasitized by a braconid wasp species. These parasitoids had a significant positive effect on seed set by preventing further seed consumption by the moth larvae (Fig. 10).



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  		Fig. 10. Frequency distribution of the number of intact seeds per fruit. (A) Phyllanthus bourgeoisii. (B) P. aeneus. Epicephala larvae were parasitized by braconid wasps. Fruits from which moths/wasps had already emerged were assigned to each category based on differences in exit-hole structure. The number of intact seeds within uninfested fruits ranged from two to six due to the presence of unfertilized/aborted ovules and/or empty, sterile seeds

 
Upon examining additional Gomphidium species, we found that Epicephala larvae infested the fruits of 20 of 25 species (Table 1) and that the seeds within these infested fruits were entirely destroyed. Of the 12 species from which we sampled female flowers, 11 contained moth eggs within pollinated flowers in proportions ranging from 25% (P. poumensis) to 95% (P. buxoides) (Table 1). In all cases, eggs were laid on the external surface of flowers, and thus oviposition by adult moths did not damage the ovary. These data indicate that the Gomphidium–Epicephala association is fairly widespread among other members of this subgenus.

We also obtained adult moths reared from the fruits of nine Gomphidium species, P. bourgeoisii, P. aeneus, P. mangenotii, P. guillauminii, P. chamaecerasus, P. koniamboensis, P. pilifer, P. vulcani, and P. pancherianus. In most cases, individual moths that developed from different hosts were easily distinguishable by wing pattern and relative size, indicating that these moths are specific to a single Phyllanthus host. The host-specificity of the moths was further supported by nucleotide sequence variations within 1317 bp of the COI gene (Fig. 11). Pairwise sequence differences between individuals collected from different hosts averaged 12% (range: 3–15%), whereas differences were <0.3% among individuals parasitizing the same host, despite regional co-occurrence of the host plants (P. bourgeoisii and P. chamaecerasus at Chutes de Ba, P. aeneus and P. mangenotii at Cap Bocage, and P. tiebaghiensis and P. guillauminii at Tiébaghi).



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  		Fig. 11. Unrooted neighbor-joining phylogram depicting relative branch lengths within and among Epicephala moth individuals collected from different Phyllanthus host species. The tree is based on uncorrected pairwise distances within 1317 bp of the mitochondrial cytochrome oxidase subunit 1 gene (COI). All the moths used in the analysis are currently undescribed, and host affiliation of each individual moth is given in parentheses. Locality information is also provided to the right of shaded bars

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Our analyses revealed that at least two species of New Caledonian Phyllanthus are pollinated actively and exclusively by Epicephala moths. The larvae of these moths consume all six ovules of the developing fruit, while leaving a fraction of the fruits intact (Fig. 10). Similar association of Epicephala moths found in majority of the Phyllanthus species examined (Table 1) suggests that the interaction between species of Phyllanthus and Epicephala is a coevolved pollination mutualism that is potentially widespread among diverse species of the subgenus, Gomphidium. Epicephala moths were shown to be highly specific to a single Phyllanthus host based on both morphology and genetic variation (Fig. 11). Although pairwise sequence differences among individuals of the same species were extremely low (0–0.3%), the level of intra- and interspecific genetic variation is comparable to that reported for Glochidion-pollinating Epicephala moths (Kato et al., 2003 ).

The most critical factor underlying the Gomphidium–Epicephala mutualism is that a fraction of the fruits is left untouched by the moths. This is most likely brought about by the absence of moth eggs in a fraction of pollinated flowers, although we have not ruled out asexual seed production (apomixis), which may also account for the occurrence of uninfested fruits. One possible explanation for the described pattern of egg distribution is that Epicephala eggs may be lost from some flowers, possibly by egg predation or strong desiccation. In some yucca–yucca moth interactions, high mortality of eggs and/or early instar larvae is an important process for limiting seed consumption by the moths (Addicott and Bao, 1999 ; Csotonyi and Addicott, 2001 ; Shapiro and Addicott, 2003 ). However, in P. aeneus, moths oviposit directly into the tissue of the calyx lobes, thereby scarring the surface of the lobes. Such scars were not observed in flowers without moth eggs, which may allow exclusion of egg mortality as an explanation.

Another possibility is that the moths do not always oviposit in flowers that they pollinate, although this cannot be concluded from our limited number of observations. Such behavior seems paradoxical, because the moths do not benefit from the pollinating behavior itself. This seemingly altruistic pollination behavior may be advantageous to the moth because presence of uninfested fruits might force the braconid parasitoid to spend excessive time in detecting a host, thus decreasing the probability of detecting and parasitizing moth larva. Weiblen et al. (2001) suggested that in functionally dioecious figs, the presence of seed figs reduces search efficiency of the parasitoids that attack pollinator wasps and hypothesized that functional dioecy leads to increased pollinator production. More detailed examinations of moth pollination and oviposition behavior as well as parasitoid searching strategy are clearly needed before this hypothesis can be evaluated robustly.

Empirical studies have demonstrated that in some obligate pollination–seed-parasitic interactions, plants selectively abscise flowers that contain large numbers of eggs, thereby preventing excessive seed destruction (Pellmyr and Huth, 1994 ; Ritcher and Weis, 1995 ; Wilson and Addicott, 1998 ; Addicott and Bao, 1999 ). In light of this, it is paradoxical that Gomphidium trees do not abscise flowers containing moth eggs, despite the substantial cost imposed by the larvae. This may be a primary source of evolutionary instability because the extent of larval damage should vary among populations and between years (Addicott, 1986 ; Thompson, 1994 ; Pellmyr and Thompson, 1996 ; Thompson and Cunningham, 2002 ), and excessive exploitation by pollinators should lead to insufficient plant reproduction. One explanation for the lack of selective abscission in Gomphidium is that the potential for such a mechanism is weak because the available resources do not limit seed set and thus need not be allocated to high-quality fruits. However, as hypothesized for some yuccas (Addicott and Bao, 1999 ), Gomphidium flowers may not have proximate cues to predict whether their ovules are infested, because oviposition by Epicephala moths does not directly damage the ovary. Selective abscission may be more likely involved in the Glochidion–Epicephala mutualism, in which the ovipositor of the moth directly cuts through the ovary and/or style tissue, and the reproductive success of the plant strongly depends on the number of eggs laid per flower (Kato et al., 2003 ).

Given that Gomphidium plants do not possess a mechanism by which to prevent excessive exploitation by Epicephala moths, there is also no means by which the pollinators can retaliate against being overexploited by the plant. Once a plant acquires the ability to selectively abscise flowers containing moth eggs, it attains higher relative fitness, which would rapidly lead to pollinator extinction. Importantly, such a pathway leading to the breakdown of the system is inherently avoided in other obligate mutualisms, because the exclusive pollinators of the plants consistently infest the flowers (or syconia) that they pollinate.

Theoretical studies have predicted that cooperative interactions are evolutionarily stable only when both participants possess mechanisms to prevent overexploitation by the other (Axelrod and Hamilton, 1981 ; Bull and Rice, 1991 ; Bronstein, 2001 ). It is therefore intriguing that a seemingly unstable interaction between Gomphidium and Epicephala has persisted through evolutionary time and has undergone extensive reciprocal diversification. The underlying principle of this system implies that mechanisms inherent to the mutualists are not necessarily responsible for the evolutionary stability of obligate interactions. Recent empirical studies on yucca–yucca moth and Trollius–Chiastocheta systems have also shown that various ecological factors, such as density-dependent mortality of moth larvae, may be more important in determining the overall costs and benefits of the mutualism (Wilson and Addicott, 1998 ; Addicott and Bao, 1999 ; Csotonyi and Addicott, 2001 ; Jaeger et al., 2001 ).

Although the proximal process generating seed set in Gomphidium plants is currently unknown, our results show that there are major differences in feeding patterns between Epicephala moths associated with Gomphidium and Glochidion fruits and that different mechanisms may be responsible for the evolutionary stability of these specialized interactions. Future studies should rigorously determine the processes regulating the costs and benefits of these mutualisms as well as factors contributing to the observed differences in modes of interaction between the two systems. Within the family Euphorbiaceae, there are several other genera that are closely related to Glochidion and Phyllanthus, such as Breynia, Sauropus, Flueggea, and Margaritaria (Webster, 1994 ). Knowledge on pollination systems of these related plant groups, combined with robust phylogenetic hypotheses of both plant and moth lineages, would further add to our understanding of the evolutionary dynamics of pollination mutualisms involving euphorbiaceous trees and Epicephala moths.


   FOOTNOTES
 
1 The authors thank the staff of Direction des Ressources Naturelles de la Province Sud and Direction du Développement Economique et de l'Environnement, Province Nord for kind help and issuing permission for research in New Caledonia. We are also indebted to A. Takimura for help in the field and laboratory. Back

2 kawakita{at}bio.h.kyoto-u.ac.jp . Back


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 MATERIALS AND METHODS
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 DISCUSSION
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K. J. Wurdack, P. Hoffmann, R. Samuel, A. de Bruijn, M. van der Bank, and M. W. Chase
Molecular phylogenetic analysis of Phyllanthaceae (Phyllanthoideae pro parte, Euphorbiaceae sensu lato) using plastid RBCL DNA sequences
Am. J. Botany, November 1, 2004; 91(11): 1882 - 1900.
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A. Kawakita and M. Kato
Obligate pollination mutualism in Breynia (Phyllanthaceae): further documentation of pollination mutualism involving Epicephala moths (Gracillariidae)
Am. J. Botany, September 1, 2004; 91(9): 1319 - 1325.
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