5. The Incredible Fig/Fig Wasp Scenario

C ertainly one of the most complicated and remarkable examples of male gender inequity is the classic disproportionate role of the male in the fig wasp life cycle. In fact, this subject is so fascinating that the staff at WAYNE'S WORD has mentioned it in several other articles.

T iny male and female fig wasps are borne inside hollow, fleshy, flower-bearing structures called syconia. [The syconium is what most people associate with the tasty fruit of a fig, but technically it is not a true fruit.] The syconium is lined on the inside with hundreds of tiny, pollen-bearing male flowers and seed-bearing female flowers, and the wasps develop from eggs laid inside the ovaries of the short-style female flowers (one egg per flower). In about half of the fig species (referred to as monoecious), male flowers and the long and short-style female flowers occur in the same bisexual syconium; but in all other fig species (referred to as dioecious or gynodioecious), the seed-producing, long-style female flowers only occur in unisexual syconia on female trees (with no male flowers). Since wasp eggs are not laid in the long-style flowers, the ovary of this type of flower contains a seed rather than a wasp (assuming it is pollinated). This remarkable floral dimorphism is how the fig tree produces seeds while still maintaining its vital, "in-house" population of symbiotic wasps. There are approximately 1,000 species of figs (genus Ficus), mostly distributed throughout tropical regions of the world, and they all have their own pollinator wasp species that only enters their syconia through a small opening (called an ostiole) to pollinate the female flowers inside. Without their special symbiotic wasps transferring pollen from one syconium to another, the female flowers inside would not get pollinated and no seeds would be produced (a catastrophe for the fig tree).

I t should be noted here that some fig species have two species of symbiotic wasp pollinators. In fact, the classic one-fig/one-wasp partnership has been challenged in an article by D. Molbo et al. (Proceedings of the National Academy of Sciences 2003 100: 5867-5872). The two fig wasp species may be closely related sister taxa, or may be quite different from each other. This indicates both long-term coexistence on shared hosts and relatively recent colonization of fig species. Fig syconia may also contain "bogus fig wasps" who do not pollinate the female flowers inside. It is clear that the fig-fig wasp scenario is far more complicated than originally described.

A close-up view inside of the rustyleaf fig syconium showing numerous minute male and female flowers. The female flowers are pollinated by a tiny pregnant (gravid) female fig wasp that enters the syconium through an opening at one end (the upper end in photo).

Magnified view of a male and female fig wasp (Pleistodontes imperialis) next to the "eye" of an ordinary sewing needle. The smaller, wingless male has an amber body and black head with greatly reduced eyes.

Close-up view of a male and female fig wasp (Pleistodontes imperialis). The smaller male (right) has a greatly reduced body which has two primary purposes: (1) Inseminating the female and (2) Drilling exit tunnels through the syconium wall.

Magnified view inside syconium of Ficus rubiginosa showing two male and two female fig wasps (Pleistodontes imperialis). The smaller males (left) have a black head and amber-colored, wingless body. The winged females (right) are larger with longer antennae. In this image, the inseminated females have imerged from their individual flowers and are ready to escape from the syconium.

Richard Dawkin's Model Of Vicarious Selection Chapter 10 of Climbing Mount Improbable , W.W. Norton & Company, 1996.

T

he staff at WAYNE'S WORD agrees with Richard Dawkins that the fig/fig wasp scenario is truly one of the most remarkable and complicated examples of coevolution between a plant and an insect; however, his fascinating discussion of vicarious selection to explain this symbiotic relationship is based on dioecious figs with separate male and female trees. About half of the world's fig species are monoecious (with male and female flowers in the same syconium) and do not fit Dawkin's model for vicarious selection. Dawkin's model is based on the paper by Grafen and Godfray ( Proc. R. Soc. Lond. 245, 1991). Vicarious refers to an act performed by one person or organism (in this case a syconium) in place of another.

A ccording to Carole Kerdelhue and Jean-Yves Rasplus (Oikos Vol. 77: 163-166, 1996), dioecious figs may have evolved from monoecious ancestral fig species due to selection pressure by non-pollinator fig wasps. Although these non-pollinator wasps belong to the same order Chalcidoidea as pollinators, many of them belong to different families. They do not benefit the fig and may even be harmful, especially when they compete with and/or parasitize the beneficial pollinator wasps. According to Kerdelhue and Rasplus (1996), non-pollinator, parasitic wasps never occur in the long-style flowers of female syconia on female trees, and non-pollinator gall-makers are uncommon in the male syconia of male trees. Therefore, seed production in female syconia and pollinator wasp production in male syconia are not diminished as in the syconia of monoecious figs with stratified ovaries containing all of the non-pollinator wasp species. In addition, no gall-makers that lay eggs through the syconium wall (after pollination by pollinator wasps) have ever been found so far in dioecious figs. These bogus fig wasps have very long ovipositors that can penetrate the entire outer wall of the syconium. For the fig, having separate male and female trees (bearing male or female syconia) in the population may have a distinct adaptive advantage with regard to pollination and seed production.

Bogus fig wasps (family Torymidae and Eurytomidae) have an unusually long ovipositor. It can easily penetrate the long-style flowers which are too long for true female fig wasps. In fact, some species can penetrate the entire syconium from the outside! Thus, bogus fig wasps can lay eggs in long-style fig flowers reserved for fig seeds. Consequently, no seeds are produced in these flowers. In addition, the bogus fig wasps do not pollinate fig flowers. Although they do not benefit the fig tree, torymid and eurytomid wasps are common inhabitants of New World monoecious fig syconia. Their coexistence with natural fig pollinator wasps is a complex and perplexing coevolutionary problem in fig biology.

A. Short-style female flowers inside male syconium of a dioecious fig. [Male flowers also occur in this syconium.] B. Long-style female flowers inside the female syconium of a dioecious fig. These syconia do not have the intermediate ovary positions of monoecious figs (see below), and they do not harbor all the non-pollinator wasp species of monoecious figs.

I n Dawkin's model, selection for wasp pollination morphology (i.e. ovipositor length, etc.) and behavior (purposive loading and unloading of pollen) is taking place in wasps who enter and leave male syconia (containing short-style female flowers) on male trees. This selection is crucial for the perpetuation of fig trees when wasps enter female syconia on female trees (which superficially resemble male syconia). Female syconia produce seeds (the vital genetic link for fig trees) and are a genetic graveyard for wasps because they cannot oviposit in the long-style female flowers. For wasps in female syconia, mutations for a longer ovipositor that could reach the ovary of long-style flowers would not be passed on. For wasps in male syconia, there is no selective advantage for longer ovipositors because they are already long enough to easily penetrate the ovary of short-style flowers.

S ome varieties of the common dioecious fig (F. carica), such as the delicious Calimyrna, have another method of blocking the development of non-pollinator bogus fig wasps. Without pollination, Calimyrna syconia fail to ripen and drop from the branches. This eliminates the life cycle of non-pollinator fig wasps that may have laid eggs in the syconium.

A lthough vicarious selection for ovipositor length may be dictated by the male syconia on male trees, there are several other pollination patterns in dioecious figs that differ from Dawkin's model for vicarious selection. See Pollination Patterns In Dioecious Figs. Dawkin's dioecious fig model fits species of dioecious figs in the subgenus Urostigma. These figs have the prerquisites for vicarious selection, including: (1) purposive pollination (pollen collecting and pollen transfer by female wasps); (2) female wasps with pollen baskets (corbiculae); (3) exit tunnels cut by male wasps, etc. But in reality, there are many fig species with passive pollination (i.e. not deliberate), without pollen baskets, and without exit tunnels cut by male wasps. In fact, it is doubtful that vicarious selection adequately explains the remarkable evolution of the numerous fig species with pollination patterns that are different from Dawkin's fig model.

M onoecious syconia of Ficus sur contain long-style and short-style female flowers densely packed together in a layer that lines the inner cavity of the syconium. Although the styles all form a relatively continuous stigmatic layer called a synstigma (i.e. all stigmas in the same plane) within the syconium, the ovaries may be deep or shallow relative to the synstigma depending on the length of their flower stalks (pedicels). Generally, the deep-seated ovaries (on short pedicels) with long styles each contain a seed, while the shallow ovaries (on long pedicels) with short styles each contain a wasp larva (referred to as a "gall flower" by some authors). A pollinator wasp walking on this "bed" of styles (synstigma) can insert her ovipositor down the short style and easily penetrate the ovary where she lays an egg. The deep-seated, long-style ovaries are out of reach for her ovipositor (style longer than her ovipositor), and consequently these ovaries develop seeds rather than wasp larvae.

B ecause of intermediate style lengths (between long and short) and different ovary heights due to the length of flower stalks (pedicels), the ovary position of female flowers in monoecious fig syconia often forms a stratification. According to Kerdelhue and Rasplus (1996), there are at least 4 different ovary layers occupied by beneficial (pollinator) and non-beneficial and/or harmful non-pollinator wasps. These layers are listed according to their position (depth) from the stigmatic surface (synstigma) within the syconial cavity. See the following illustration.

Heterostyly and four ovary layers (stratification) within the syconium of a monoecious fig (Ficus sur). (1) Yellow: The most shallow ovaries (near surface) with shortest styles which typically contain a pollinator wasp larva; (2) Green and (3) Red: Slightly deeper ovaries that typically contain non-pollinator wasp larvae; (4) Black: The deepest ovaries with longest styles that typically bear mature seeds. 1. The shallow ovary layer of short-style flowers (yellow ovaries in above illustration) are mostly occupied by larvae of wasps that oviposit from the synstigma within the syconium cavity, including Ceratosolen (pollinator) and Sycophaga (non-pollinator gall-maker), and by their parasitic wasp larvae (parasitoids or inquilines). 2. A second slighter deeper ovary layer (green ovaries in above illustration) includes the wasps of layer 1 (above) plus some additional gall-makers which lay eggs from the outside (Apocryptophagus). 3. A third deeper ovary layer (red ovaries in above illustration)) produces a few seeds and provides shelter and food (galled endosperm tissue) for mainly Apocryptophagus and a few Sycophaga individuals. 4. A fourth, deepest ovary layer (black ovaries in above illustration) produces mostly seeds and some wasps, including some Sycophaga and a few Apocryptophagus. If the non-pollinating wasps are very numerous, the medium layers 1 and 2 (yellow and green ovaries) will be occupied entirely by exploiters and these occupied flowers will not produce seeds or pollinator wasps. According to Kerdelhue and Rasplus (1996), this probably represents a high cost to the fig with regard to seed production.

T he following scenario occurs three or more times a year (depending on the fig species). The example used in this discussion is essentially based on the monoecious Australian rustyleaf fig (Ficus rubiginosa) and its symbiotic pollinator wasp (Pleistodontes imperialis). About three months after the wasp eggs are laid inside short-style flowers by the mother wasp, the mature male wasps emerge first--each male chewing his way out of the ovary he was borne in. Compared to the larger winged female (another example of sexual dimorphism) he is a minute, wingless wasp with greatly reduced eyes and a reduced, feeble body. In fact, he can barely walk, clumsily moving around inside the syconium in search of a female. Actually he really doesn't need wings, running legs or eyes because his short adult life on this earth is totally within the confines of his dark and dingy syconium. For his reduced size, he does have strong little mandibles (jaws) which come in very handy in the two major roles of his short life cycle:

Male Role #1.

H e crawls to a short-style female flower that contains a mature female wasp. He climbs up on the ovary of the flower, bites a fertilization hole in the ovary wall, and inserts his long, slender rear end (abdomen) into the opening (and into the wasp's vagina), thus inseminating a female who really never sees who is mating with her. Each male repeats this process with every female they find, as they slowly move through the dense "jungle" of long and short-style female flowers. After being inseminated the female crawls out of the fertilization hole through the ovary wall initially made by the male. At this precise time the male flowers have reached maturity and are shedding pollen. The female wasp purposively (deliberately) collects pollen from the male flowers and packs it into a pair of little pollen baskets (corbiculae) on the underside of her thorax. In many fig species (especially dioecious figs) she simply collects pollen passively (not deliberately) in the folds and crevices of her exoskeleton as she moves through dense, pollen-laden male flowers. It is difficult to generalize about pollen-collecting behavior because it varies considerably within the incredibly complex subgenera of Ficus.

A male fig wasp (Blastophaga psenes) mounting a short-style female flower and inserting his long, slender abdomen into a fertilization hole that he cut through the ovary wall to inseminate the female fig wasp inside.

A female fig wasp (Pleistodontes imperialis) emerging from a short-style female flower. She enlarges and pushes through the fertilization hole in the ovary wall cut by the male.

Male Role #2.

A t this time the male wasps begin tunnelling through the syconium wall, chewing away at the tough outer layer. These exit tunnels are absolutely crucial in order for the female wasp to escape. Again, the exact method of wasp exodus depends on the subgenus of Ficus. In some species, the ostiole where the original mother wasp entered to lay her eggs months earlier, actually opens again, thus allowing the pregnant (gravid) female wasps to escape. Here is one of several examples given by Richard Dawkins in Climbing Mount Improbable page 309 (1st paragraph) that just doesn't fit: "A male that did sit back and let his colleagues make the hole would be able to save up all his energy for mating with females, secure in the knowledge that he need not hold himself back for the effort of making the hole." In every fig species we have studied (either from direct observations of live wasps or from the literature), the males mate with the females before the tunnels are cut. In fact, according to Dr. J. Galil, the famous fig biologist at Tel Aviv University (Endeavour Vol. 1, 1977), all the respiratory activity of male wasps (during mating and tunnelling) increases the carbon dioxide concentration within the syconium (up to 10 percent or three times the atmospheric level in Ficus religiosa). Upon completion of the exit tunnels, the carbon dioxide level drops rapidly as the gas escapes into the outside atmosphere. The depletion of carbon dioxide activates the female wasps, causing them to enlarge the fertilization holes and push through the ovary walls of the individual short-style flowers they were born in. And of course there are many fig species that do not even have (or need) exit tunnels cut by males, the females simply exit through the main ostiole at the end of the syconium. In these latter species, the feeble males have essentially only one primary role (see role #1 above), that is, to inseminate the female.

Circular exit tunnels in the mature syconium wall of the rustyleaf fig (Ficus rubiginosa). The tunnels were cut by the male fig wasps to enable the winged females to escape. Soon after the tunnels are cut, the tiny males die, their purpose in life having been fulfilled. Without the exit holes, the females would perish inside the syconium, along with their male sex partners and liberators.

T he exiting female wasps emerge from the neat circular tunnels cut by the males and fly off to other receptive syconia to lay their eggs, and the whole cycle starts all over again. With their purpose fulfilled, the tiny males soon die within the syconium, never leaving the place of their birth and sexual orgy. At this stage the syconium becomes juicy and sweet, and may serve as food for hungry monkeys and bats high in the rain forest canopy. This final phase is also important for the fig tree because it insures that seeds contained inside long-style flowers are deposited to other places (due to the purgative effect on the animals digestive tract). Many of these amazing tropical figs start growing as epiphytic vines on the host tree's limbs, soon reaching the ground where they develop extensive root systems. Like a botanical boa constrictor, these "strangler figs" eventually envelop the host tree as their tangled masses of snake-like vines fuse (anastomose) into a massive trunk.

A lthough a number of testosterone-laden, male general biology students have said (jokingly) that they envied the male fig wasp, his short wasp life is basically limited to a brief sexual orgy within the stuffy syconium (with the exception of those figs that require exit tunnels through the syconium wall). But even though his role may seem limited and seemingly insignificant, the tiny male fig wasp is absolutely essential for the perpetuation of fig wasps and fig trees in one of nature's most successful symbiotic relationships.