674 Experientia 45 (1989), Birkhduser Verlag, CH-4010 Basel/Switzerland Reviews Ecological and evolutionary dynamics of fig communities

S. A. Frank Department of Ecology and Evolutionary Biology, University of California, Irvine (California 92 717, USA)

Summary. I review the status of five topics in fig research: pollen-vector versus seed production, flowering phenology and wasp population dynamics, monoecy versus dioecy, parasite pressure, and fig wasp behavior. I raise several new questions based on recent research on two components of fig reproduction : pollen-donation (male) and seed-produc- tion (female) success. I focus on how these two components of reproductive success depend on the flowering phenology of the figs and the population dynamics of the pollinator wasps. Key words. Coevolution; comparative method; development; Ficus; fig; Hymenoptera; mutualism ; parasite; pheno- logy; phylogeny; pollination.

Introduction contrast, syconia entered later tended to have few foundresses, to be large, and to have a high fraction of In 1979 three important papers on fig research were pub- seeds relative to wasps. Because of within-crown syn- lished. Wiebes " surveyed work on phylogenetic recon- chrony of syconium maturation and of wasp arrival, in- struction of figs and their pollinating wasps, with an dividual crops tended to produce syconia that varied emphasis on coevolutionary history as revealed by phy- little in size and in relative wasp versus seed production, logeny. Hamilton " noted that the unusual life cycles of whereas there was much variation among crops. Single pollinator and parasite fig wasps have caused three con- crops therefore tended to be relatively more successful as vergent characters to evolve repeatedly and independent- pollen donors when entered early and as seed producers ly: wingless males, lethal combat among males, and male when entered late. Total success per syconium, seeds plus dimorphism in which some males are winged and others female wasps, was considerably lower for crops entered are wingless. Janzen 23 provided an overview of many relatively early during the period of receptivity. ecological and evolutionary questions regarding the These general trends in wasp versus seed production oc- wasp-fig symbiosis, including aspects of flowering phe- curred both spatially, among different trees, and tempo- nology, relative seed and wasp production per fig, and rally, among different crops on the same tree. By collect- wasp movement. ing both spatial and temporal data, Bronstein was able to When these three papers were written, there were just conjecture that the observed patterns are caused by de- enough data available to sketch out important questions velopmental variation common to all individuals rather for future study. Some progress has been made recently than by genetic variation among individuals 4' 5. on a few questions and, of course, many new questions This hypothesis about the developmental basis of ecolog- have been raised. In this paper I will briefly summarize ical correlations was tested more stringently by experi- new observations and the current status of five topics in ment. Bronstein 4 bagged different branches of the same fig research. I will rely on the 1979 papers for biological tree and introduced wasps at different stages of syconium background and detailed reference lists on past work. receptivity. Variation among experimental branches within trees was as great as variation among crops en- tered at different stages, suggesting that most observed Wasp versus seed production variation was caused by an interaction between develop- mental processes and variation in wasp abundance. A monoecious fig inflorescence (syconium) contains hun- Herre 2° compared numbers of flowers, foundresses, dreds of pistillate and fewer staminate flowers. Each pis- wasps, and seeds per syconium among 12 species of mo- tillate flower eventually produces one seed, one wasp, or noecious figs (subgenus Urostigma) in Panama. He sug- nothing. Pollen is dispersed only by female pollinator gested that these fig species can be ordered along a con- wasps, so the number of female wasps produced indicates tinuum, from those with a small number of flowers, the plant's success through male reproductive function. which produce relatively low proportions of viable seeds The number of seeds per syconium indicates success and high proportions of female wasps, to those with a through female function. large number of flowers, which produce relatively high Bronstein"' 5 studied naturally occurring spatial and proportions of viable seeds and low proportions of fe- temporal variation in the numbers of wasps, seeds and male wasps. These observations imply an evolutionary empty ovaries per syconium in Ficus pertusa in Costa and perhaps adaptive trend among this suite of charac- Rica. Syconia that were entered by female pollinator ters. wasps (foundresses) early during their period of receptiv- An independently derived estimate of phylogeny might ity tended to have many foundresses, to be small, and to suggest possible explanations for the observed covaria- produce a high proportion of wasps relative to seeds. By tion among these characters. For example, there may be Reviews Experientia 45 (1989), Birkhauser Verlag, CH-4010 Basel/Switzerland 675 a continual trend toward larger or smaller flower number Herre observed that, among species, syconia with fewer throughout the complex of Urostigma occurring in this flowers have relatively fewer foundresses. This may de- area, suggesting a strong directional selection pressure on pend on differences in wasp density among species, with flower number or some correlated character. By contrast, smaller syconia associated across species with low wasp if flower number is independent of phylogeny, then each density. Herre suggests that circumstantial evidence is species may be adapted to, for example, its own environ- against this explanation 20 . An alternative and testable mental conditions and mode of dispersal. developmental explanation is that species with a relative- Comparisons within species across their geographic ly short period of flower multiplication, leading to fewer range would be an interesting supplement to Herre's flowers, also have relatively shorter periods for foundress data. Several Urostigma species are, according to current entry after the first arrival (3), leading to fewer found- taxonomy, distributed through the Caribbean islands to resses per fig. Panama and from Mexico southward through Central Another pattern likely to occur is variation in syconium America 2 . One could use geographic distance as an size among species that have a similar number of flowers. indication of the phylogenetic distance among popula- In this case the period of foundress receptivity may be tions within species, or if possible, resolve the phylogeny shifted later in those species with larger syconia (2), since of populations within species by morphological and bio- syconia appear to increase in size when foundresses enter chemical characters. If, for example, fig size and related relatively late in development 4' 5. characters of a single species increased steadily across its Studies of syconium development, such as those pio- range, in a manner typical of clines, or according to some neered by Verkerke will be important for determining a priori prediction concerning development or adapta- the role of the three timing characters in both ecological tion, then one may hypothesize particular processes to variation within species and evolutionary divergence guide further experimental and comparative studies. At among species. the end of this section I propose one plausible adaptive The tree developmental processes suggest how variation explanation for variation in syconium size among spe- is formed. The striking range Herre 2° observed in syconi- cies. um size (dry wt : 0.05 –2.6 g) and flower number (180 – There is an interesting contrast between Herre's 2° 2051) among twelve species in one location suggests that among-species and Bronstein's 6 within-species data : potent selective forces act on variation in syconium char- among species, smaller compared with larger syconia acters. I suggest that competition for seed dispersers tend to have fewer flowers and fewer foundresses, where- leads to adaptive character displacement in syconium as within Ficus pertusa, smaller compared with larger size, with each size category of fruit favored by different syconia have similar numbers of flowers but more dispersers. foundresses. These contrasting patterns may be framed Grant 13, 14 has reviewed the problems of testing charac- within a developmental context. In particular, syconium ter-displacement hypotheses. One simple approach development and receptivity to foundresses can be de- would be to partition variation among species in fruit size scribed by three timing mechanisms : 1) the period during and other syconium characters into variation within lo- which flower primordia multiply and flower number is cations and among locations. If variation within loca- determined; 2) the onset and subsequent period of recep- tions is greater than expected by chance, then divergent tivity to foundresses relative to the developmental stage selection pressure on syconium characters is implicated. of other syconium characters, including overall size (see Many alternative explanations would of course remain, above); and 3) the amount of time between the first entry and these would have to be sorted out by analyzing phy- by a pollinator and the sealing of the ostiole. logenetic and biogeographic history. The developmental causes for among- and within-species trends can be explained in terms of these three timing characters of syconia. a) Among-species variation. The Population dynamics of figs and pollinating wasps species-specific range of flower number is determined early in development by mechanism (1). The temporal In the previous section I described how pollinator wasp window of foundress receptivity relative to the develop- density affects the ratio of wasp to seed production per mental stage of other syconium characters sets the range syconium. What determines wasp density? The interde- of syconium size for a fixed number of flowers (2). pendence between wasp and fig life cycles makes this b) Within-species variation. High wasp density will lead question particularly interesting. Pollinator wasp species to foundresses entering early during the window of are, in general, restricted to a single fig species, and figs foundress receptivity (2) and to many foundresses arriv- usually have only one pollinator species 39 . When wasps ing at each syconium during the fixed entry period after emerge from a syconium they must find a receptive syco- the first arrival (3). This yields a negative correlation nium to enter within a few days or else perish. A short between syconium size and wasp density during receptiv- gap in the population-wide flowering of a fig will there- ity. This within-species prediction remains to be tested on fore cause local extinction of its pollinator wasp. In Herre's species. general, the spatial and temporal pattern of flowering

676 Experientia 45 (1989), Birkhauser Verlag, CH-4010 Basel/Switzerland Reviews (phenology) of the figs determines wasp population dy- ties would be more likely to have within-crown asyn- namics. chrony than populations or species at high density. Several questions arise concerning wasp population dy- Bronstein reviewing more recent data, concluded that namics and fig flowering phenology. How can a pol- although within-crown asynchrony does occur in some linator wasp population be maintained if a constant marginal populations, it also occurs in areas that are source of receptive syconia are needed? What are the likely to have high plant densities. She proposed a mod- dynamical properties of wasp population size? What are ified version of Janzen's explanation : within-crown asyn- the sources of phenological variation within fig popu- chrony may reduce the number of individual plants lations? What causes phenological variation among spe- required to prevent a temporal flowering gap and polli- cies? nator wasp extinction. Bronstein's explanation does not In this section I consider only monoecious figs, since very require within-crown wasp transfers, which depend on a little data are available for comparison among dioecious very particular timing of wasp receptivity and emergence. species. For a discussion of phenology in a dioecious I propose an alternative explanation for within-crown species, see Kjellberg et al. 26. asynchrony. Individual plants may be resource-limited I begin by considering the sources of phenological varia- when all syconia of a synchronous crop get pollinated, tion within populations and the effects of this variation whereas a plant may be pollen-limited when pollinator on wasp population dynamics. Population phenology density is low. Selection favors asynchrony because it can be described by the number and spatial location of reduces the probability of either extreme. Within species, syconia at a particular developmental stage for each day a developmental process that caused increasing within- of the year. Population-wide pattern can be partitioned crown asynchrony with increasing resource stress would into two levels. First, the temporal correlation among be consistent with this adaptive scenario. Among species, syconia within an individual crown describes the amount consistently high or low pollinator density would be of individual synchrony or asynchrony. Second, the tem- equally likely to favor asynchrony. poral correlation among individuals describes seasonal Turning now to the timing of flowering among plants, the flowering variation and the degree of population-level population-wide flowering peaks observed in some spe- asynchrony among individuals. cies ' 0' 40 seem fairly easy to explain. Seed dispersers, Fig phenology is often described as synchronous within water, light and nutrients typically have annual cycles each crown of an individual and asynchronous among which probably favor flowering and fruiting cycles. A individuals. This trend is often observed, but is not a more difficult question is why some plants would flower general rule and is, at present, poorly quantified. when conditions are poorer than during these seasonal Janzen 23 and Bronstein 6 discussed asynchrony within peaks. Certainly there will be fewer plants competing for crowns, and Milton et al. 30 and Windsor " described available pollinator wasps during off-peak periods, al- tendencies toward population-wide flowering peaks in though there will also be fewer wasps except during the several Panamanian species. period following the flowering peak. Likewise, there will Within-crown asynchrony can have profound effects on be fewer plants competing to donate pollen, but also pollinator population dynamics and patterns of pollina- fewer receptive plants except as the population moves tion because it can allow wasps simply to move from one toward its flowering peak. Parasite pressure is also likely part of a tree to another 23 . A single tree would thereby to diminish during the off-season (see later section on maintain a private population of pollinators, avoiding Parasitoids, seed predators and inquilines'). pollen limitation and generally suffering the usual costs One hypothesis is that annual flowering patterns are in- and enjoying the usual benefits of inbreeding. The prob- fluenced by frequency-dependent competition for ob- lem for figs is more interesting, however, because a tree taining pollinating wasps and for donating pollen 27.The that manages to maintain wasps during a period of frequency-dependent hypothesis makes a specific predic- sparse flowering can be a very successful pollen donor tion : the combined seed dispersal and pollen donation when other plants enter a flowering peak. success of each plant, matched for size and resource Janzen 23 pointed out that only a few asynchronous syco- availability, will on average be equal throughout the nia within a crown can have a significant effect on pollen year. If this were not so, then selection would favor mod- flow and wasp population dynamics. For example, if ification of plants that were performing worse than aver- each tree were absolutely synchronous within its crown, age. The equality of success is, at least in principle, a then many trees flowering asynchronously would be testable hypothesis. This hypothesis can be called 'adap- needed to guarantee a constant source of receptive syco- tive,' since it assumes that phenotypes have been molded nia in a local population. By contrast, if some trees had primarily by factors that affect reproductive success, a few asynchronous syconia timed in a way that wasps such as parasites and density-dependent competition for could emerge from and reenter syconia within crowns, pollen and seed dispersers. then far fewer trees would be needed to maintain a polli- A developmental scenario could also explain population- nator wasp population. Following this logic, Janzen 23 wide flowering patterns among individuals. Suppose that hypothesized that marginal populations with low densi- plants flower whenever they have acquired enough re-

Reviews Experientia 45 (1989), Birkhduser Verlag, CH-4010 Basel/Switzerland 677 sources. If the environment is seasonal, then plants species in which sociality varies with ecological condi- would tend to acquire resources seasonally and flower in tions, suggest which factors favor eusociality. a partly synchronous manner. In an aseasonal environ- This approach to studying the origins of eusociality sug- ment plants would flower asynchronously. gests that the origins of dioecy can be analyzed by mea- Developmental mechanisms can be inferred by ecological suring variation in wasp versus seed production in mo- and experimental studies within species. For example, noecious species 20 (see above section on 'Wasp versus repeated sampling of single individuals can establish seed production'). Within monoecious species, certain whether resource level, size, or other ontogenetic proper- traits may favor relatively greater wasp production and ties affect flowering, and whether individuals have a sea- pollen donation compared with seed production and dis- sonal rhythm. Windsor's 40 study of Panamanian species persal. For example, producing more and perhaps did show a tendency for larger individuals to flower more smaller syconia per crop, flowering more frequently, and frequently (see also Milton "). Michaloud ' 9 studied the not using resources to ripen fruits and attract dispersers phenology of half-sibs of Ficus natalensis planted in a may yield higher pollen donation success and lower seed common garden. He found no effect of genotype on dispersal than producing fewer and perhaps larger syco- flowering pattern, and no seasonal rhythm within indi- nia that are more attractive to dispersers. Measuring the viduals. amount of dimorphism within populations for these two The developmental and adaptive hypotheses are not nec- strategies and the successes of each will indicate the ten- essarily alternative explanations for asynchrony among dency toward dioecy within monoecious species. Com- individuals. For example, the proposed pattern of devel- paring the amount of dimorphism among species may opment may be an adaptively evolved proximate mecha- also suggest hypotheses about the ecological factors that nism that determines how equality of reproductive suc- favor the origins of dioecy. cess is achieved. On the other hand, closely related Dioecious figs appear to cope with seasonal environ- species may share the same developmental pattern, which ments better than monoecious species (review in Bron- constrains some of these species from evolving develop- stein 6)• This observation provides very little information mental patterns that would otherwise be favored by se- about the origins of dioecy, and whether dioecy is an lection. adaptation for seasonality. A much more interesting and tractable problem is the patterns of biogeographic radia- tion found in monoecious and dioecious figs and the adaptive trends found within each group. For example, Monoecy versus dioecy one could compare trends in phenology and seed disper- In the previous two sections I discussed wasp versus seed sal syndromes within monoecious and dioecious lineages production and flowering phenology in monoecious fig with similar biogeographic histories. Evolutionary pat- species. These two factors interact to determine an indi- terns in radiations into increasingly seasonal environ- vidual plant's male and female components of reproduc- ments might suggest how monoecious and dioecious figs tive success. Within monoecious populations particular respond differently to seasonality. crops will sometimes be relatively more successful as a A clue about the role of seasonality in the origins of male (pollen donation) and sometimes relatively more dioecy may be obtained from monoecious species. Con- successful as a female (seed dispersal) 4' 5 . Whether differ- sider a monoecious species with a population-wide flow- ent individuals specialize in male versus female function ering peak. Plants that flower between peaks can con- is unknown. tribute heavily as pollen donors if they release many In dioecious species separate individuals specialize in wasps in the peak period of flowering. In particular, making either only seeds or only wasps, and the two plants flowering between peaks may maintain wasp pop- types are morphologically distinct. Although roughly ulations while expending a small amount of resource by one-half of all fig species are dioecious, dioecy has appar- flowering asynchronously within and among individuals, ently evolved from monoecious ancestors only twice 2 with small crop sizes and little investment in attracting (but see Ramirez 34). Phylogenetic comparisons and bio- seed dispersers. As the population enters its flowering geography therefore provide only limited information peak, the plants that flowered in the off-season may pro- about the origin of functional dioecy. duce a larger crop and release many pollen-carrying The difficulty of studying the origins of dioecy is similar wasps. to the problem of inferring factors that promoted the This pattern, in which pollinators are maintained at low origin of eusociality in insects : existing species have obvi- density in the off-season and then built up before the ously been modified since the time of evolutionary tran- seed-dispersing trees flower, is similar to Kjellberg et sition, and only a small number of transitions actually al.'s 26 description of the phenology of male trees (capri- occurred. Insect species that currently exhibit some prim- figs) in the dioecious edible fig Ficus carica. F citrifolia in itive social traits have been useful for comparing hy- Florida may be a good monoecious species on which to potheses about origins. In particular, closely related lin- test this scenario, since it appears to have a distinct flow- eages that vary in degree of sociality, or individual ering peak in May-July (pers. obs.).

678 Experientia 45 (1989), Birkliduser Verlag, CH-4010 Basel/Switzerland Reviews Parasitoids, seed predators and inquilines tor parasitoids or kill pollinators while competing for seed tissue and affect only male success. Morphological Each fig species maintains a large community of and phenological traits that help to avoid one or the inquiline arthropods, including nematodes, mites, other of these inquiline types may favor sexual dimor- dipterans, and several families of chalcidoid phism in the figs. wasps 3, 23, 28, 35, 38. Little is known of these inquilines The type of ostiole and wall thickness of syconia may concerning their natural history, ecological dynamics of also be shaped by seed predators and parasitoids. For populations, or evolutionary affinities. Some wasp spe- example, selection may favor divergence of these charac- cies are probably seed predators, reducing the female ters among species that have overlapping ranges, thereby component of fig reproductive success. Others are para- minimizing the success of generalist inquilines. If this sitoids of the pollinator wasps, reducing male reproduc- were the case, then these characters would vary more tive success. Finally, some are probably commensals and within a locality than predicted by a null model based on have little effect on reproductive output ' phylogeny and estimates of ancestral character state. Data on distribution and abundance of inquilines are too Along these lines, dioecious species may originally have sparse at present to draw any empirical conclusions. been very good at escaping the abundant inquilines of Anecdotes suggest that wasp inquilines may, at particu- monoecious species. For example, a dioecious species lar times and locations, be more abundant in syconia with a seasonal flowering cycle may not produce any than pollinator wasps, whereas at other times and loca- seeds over several months, which would prevent seed tions the inquiline wasps may be rare. predators from easily radiating from monoecious species. These inquilines have a potentially large effect on total This idea is difficult to test, but evolutionary patterns of reproductive success, and different inquiline species very parasite radiation onto dioecious species and the current likely have a differential effect on male and female com- overlap of parasites between co-occurring monoecious ponents of success 12 . I suggest that these inquilines may and dioecious species may be informative. Obviously, be a potent selective pressure shaping fig phenology. work on inquiline biology and phylogeny is needed 35 ' 38. If costly inquiline loads are reduced for individuals that flower away from a population-wide peak, then these Wasp behavior reproductive advantages may partly explain why some individuals do flower at times when resources such as In the previous sections I have focused on factors that light, water, and seed dispersers are relatively low. One influence the reproductive success of figs, including polli- cost of flowering at off-peak times may be a reduction in nator and inquiline population dynamics. These fig asso- available pollinator wasps. This comparison between the ciates' reproductive biology, morphology and popula- benefits of reduction in inquiline load and the costs of tion dynamics are in turn influenced by many fig traits. reduction in available pollinators raises an interesting To obtain a full understanding of fig biology and the fig question. Do population sizes of pollinators and inqui- community we must understand the ecology and evolu- lines respond differently to the changing availability of tion of these associates. On the whole, very little informa- receptive syconia? tion is available. Here I will briefly mention some inter- If inquilines were more sensitive than pollinators to low esting areas of research that have emerged from syconium abundance, then one would expect lower den- preliminary studies. sities of inquilines in the off-season and a consequent Complex morphology and behavior are often associated reproductive advantage for flowering during the off-sea- with pollen transport. The particular morphological son. I expect that hymenopteran inquilines are indeed structures and motor patterns vary widely 32' 33 . At pres- more sensitive, since a female lays only a few eggs in each ent only a few complete descriptions of behavior and syconium by ovipositing through the outside wall, where- morphology have been published (reviewed by Frank 8). as a pollinator wasp lays many eggs in each syconium. Mechanisms of pollen transport may influence the num- The oviposition pattern of inquiline wasps suggests that ber of pollinators required to pollinate a given number of specialists on a single species will be more sensitive to flowers in a single syconium. As discussed above, the population crashes of figs than generalists. Within-crown number of pollinators per syconium varies widely among asynchrony is another interesting dimension affecting the species, may vary temporally and spatially within popu- population dynamics of pollinators relative to inquilines. lations, and may influence and be influenced by develop- Synchronous crowns probably allow inquilines more eas- mental characters of the syconium. ily to find syconia at the proper stage for oviposition Oviposition behavior is another important trait. For ex- because they often use more than one syconium, whereas ample, style width may be more important than length in pollinators use only one. determining if a wasp can successfully reach the ovary Inquilines may also play a role in shaping sexual dimor- and lay an egg 36 . If true, this fact bears on the evolution phism and a tendency toward dioecy. Some inquiline of ovipositor length, flower number, style-length poly- species probably specialize as seed predators and affect morphism, and patterns of wasp versus seed production. only female success, whereas others specialize as pollina- Descriptions of oviposition and pollination are also

Reviews Experientia 45 (1989), Birkhauser Verlag, CH-4010 Basel/Switzerland 679 needed to understand the diversity of developmental pro- several species. Theory suggests that the number of in- cesses of the syconium that Verkerke 37 has recently de- quiline females ovipositing in each syconium will influ- scribed. ence the amount of sex ratio bias and wing polymor- The behavioral mechanisms by which pollinator wasps phism 16,17 The conditions leading to fighting, biased find host plants and choose to enter a particular syconi- sex ratios, and wing polymorphisms are of general inter- um influence the distribution and abundance of pollina- est in evolutionary biology. Figs and their inquilines tors. Once again, few data are available. If one watches provide an excellent system for studying these problems pollinator wasps on a receptive tree, it appears that (see Murray 31 for an interesting study of male fighting, choice is being exercised over which syconium to enter. and Godfray 12 for interesting details on both pollinator Janzen 24 suggested that wasps avoid syconia that have and inquiline sex ratio and biology). already been entered. Frank 7 found by experiment that this is true, but the mechanism is better described by the closing of the ostiole after the first wasp has entered – Conclusion that is, the tree prevents the wasps' entry. Pollinators of Ficus citrifolia in Florida did not discriminate between I have proposed several hypotheses about the ecological syconia that were recently entered and those that had interactions among figs, pollinator wasps, and the many never been entered, but avoided and appeared to have arthropod species associated with each fig species. These difficulty penetrating into syconia that had been entered ecological interactions have a strong effect on fig repro- a day earlier. Other aspects of pollinator choice include ductive success, often creating divergent selective pres- discrimination among fig species 4' 7 and discrimination sures on male and female components of success. These between syconia in which inquilines have or have not selective pressures are, in turn, partly responsible for oviposited 7. the evolutionary diversity of Ficus and its associated Sex ratio of the pollinator wasps also influences their arthropods. population dynamics, since population growth depends The observed diversity in fig traits invites speculation on the number of females. Pollinator sex ratios have about the underlying developmental processes and selec- received much attention recently. Hamilton 16 and tive pressures that have caused this variation. I have Herre 18 made comparisons within populations and attempted to frame possible explanations in terms of showed that foundress number is positively correlated both developmental and selective processes, and in a way with the frequency of males produced in a syconium. that is amenable to empirical study. New hypotheses and Kjellberg and Frank 9 found similar results based on future empirical work will be most useful if they simulta- experimental manipulation of foundress number. neously address developmental processes, components of Herre 19 found, by comparison among species, that vari- reproductive success, and variation among species. These ation in foundress number predicted the degree of devel- three types of data are, of course, what are needed for opmental plasticity in sex ratio within species. most kinds of evolutionary problems. Figs taunt seduc- Sex ratio biases depend on patterns of male competition tively with the promise that all three types of data can for access to mates '. The wingless pollinator males readily be obtained. search for mates in the confined cavity of the syconium Acknowledgments. I thank Walter Appleby, Elena Alvarez-Buylla, Judie during a limited period of time. In many fig species, one Bronstein, Allen Herre, Finn Kjellberg, and Shahid Naeem for helpful or more males chew an exit tunnel through the wall of the discussion. This work was supported by a Miller Research Fellowship in syconium, which causes the mated females to leave the the Department of Zoology, University of California at Berkeley. syconium. This situation favors a group of brothers to 1 Avila, M. V., Figs and fig-wasps native to south Florida and their find and mate with females as rapidly as possible and affinities: biogeography and taxonomy. (1989) manuscript. 2 Berg, C. C., Classification and distribution of Ficus. Experientia 45 then chew the exit tunnel. Little work has been conducted (1989) 605-611. on male movement. Frank 1 ° did find that males associ- 3 Boueek, Z., Watsham, A., and Wiebes, J. T., The fig wasp fauna of the ated themselves during mating in a way consistent with receptacles of Ficus thonningii (Hymenoptera, Chalcidoidea). Tijd- schr. Ent. 124 (1981) 149-233. the formation of brother bands, although he discussed 4 Bronstein, J. L., Coevolution and Constraints in a Neotropical Fig- alternative explanations. S. Maurice (pers. comm.) found Pollinator Wasp Mutualism. Ph. D. Dissertation, University of Mich- that, in Ficus citrifolia, igan, Ann Arbor 1986 only a few of the males inside a 5 Bronstein, J. L., Fruit production in a monoecious fig : consequences syconium chew the exit hole, and they do so before all the of an obligate mutualism. Ecology 69 (1988) 207-214. females have been mated. Conducting experiments on 6 Bronstein, J. L., A mutualism at the edge of its range. Experientia 45 (1989) 622-637 these questions is simple 1 °. Maintaining lines of wasps so 7 Frank, S. A., Theoretical and Empirical Studies of Sex Ratios, Mainly that relatedness can be manipulated will be a valuable in Fig Wasps. Master's Thesis, University of Florida, Gainesville method in future work 7' 9. 1983. 8 Frank, S. A., The behavior and morphology of the fig wasps Pegosca- Little work has been done on the behavior and popula- pus assuetus and P. jimenezi: descriptions and suggested behavioral tion dynamics of inquiline wasps. Hamilton 16 reported characters for phylogenetic studies. Psyche 91 (1984) 289-308. some sex ratio data and stressed the widespread occur- 9 Frank, S. A., Hierarchical selection theory and sex ratios. II. On applying the theory, and a test with fig wasps. Evolution 39 (1985) rence of fighting and wing polymorphism in males of 949-964. 680 Experientia 45 (1989), Birkhduser Verlag, CH-4010 Basel/Switzerland Reviews

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