Dioecious Fig Research Articles

Partial avoidance of female inflorescences of a dioecious fig by their mutualistic pollinating wasps

Every dioecious species of fig is pollinated by a specific wasp that only reproduces within the inflorescences of male trees. Pollinators usually die within the closed urn-shaped inflorescence (fig or syconium) they visit. Thus pollinators that enter female syconia allow seed production but die without reproducing. In a previous study, pollinators of one dioecious fig where male and female trees flower synchronously, Ficus hispida, did not exhibit differential attraction or choice between inflorescences of the two sexes. Here we show that Blastophaga psenes, the pollinator of another dioecious species of different lineage, the common fig (F. carica), significantly avoided female syconia, when we experimentally induce a situation of choice. Paradoxically, choosiness can be demonstrated in F. carica where usually wasps do not face a choice because male and female trees do not flower synchronously. We discuss how the mutualism may be stable despite this discrimination and hypothesize why the two species of fig-pollinators exhibit different behaviour on dioecious figs.

The Evolution of Dioecy among Ficus (Moraceae): An Alternative Hypothesis Involving Non-Pollinating Fig Wasp Pressure on the Fig-Pollinator Mutualism

In Ficus (Moraceae), about half of the species are monoecious and half are (gyno)dioecious. With a few exceptions (Kerdelhu6 et al. 1996, Rasplus in press), each is specifically associated with one single pollinating chalcid wasp (Chalcidoidea: Agaonidae: Agaoninae), which in turn only breeds on that fig species (Wiebes 1963). In monoecious Ficus species, the figs (or syconia) produced by all the trees contain both male and female flowers; the latter are set out in three or more ovary layers and have styles of various lengths. When the pollen-loaded female wasp enters the fig cavity, it lays eggs through the styles in the upper ovary layer (i.e. in the flowers with styles that are short enough for the ovipositor to reach the ovule) and pollinates the deepest flowers (Galil and Eisikowitch 1971). Basically, the outermost ovary layer will turn into seeds, whereas the inner ones will be transformed into galls and shelter pollinator larvae. By the time the wasp offspring emerges from the galls in the fig cavity, the male flowers reach maturity. When escaping from the syconium, the female wasps will bring pollen out, up to a young receptive fig. In dioecious Ficus, half of the trees bear figs that only contain one or two layers of long-styled female flowers. When the female wasp enters the cavity, it can pollinate but is not able to lay any egg. These figs will produce seeds, but no pollinators or pollen grains: such trees are functionally 'female' (Berg 1984). The rest of the trees produce figs with one or two layers of short-styled flowers, as well as male flowers. The wasp will thus be able to lay eggs in all ovaries, and its offspring will disseminate the pollen. These figs will produce pollen and pollinator wasps, but almost no seeds; such trees are functionally 'male'. In addition to its mutualistic partner, each Ficus species is associated with a great diversity of non-pollinating chalcid wasps (Hamilton 1979, Janzen 1979, Bronstein 1991, Compton and Van Noort 1992, Hawkins and Compton 1992, Boucek 1993), mostly belonging, like the pollinator, to the Agaonidae family (Boucek 1988). These wasps may be numerous (up to thirty species: Compton and Hawkins 1992), and mostly breed in the fig flowers. Some are gall-makers, and oviposit in vacant ovaries; they lay eggs either from the fig cavity at the same time as the pollinator, or from outside the fig thanks to a long ovipositor. Most of these oviposit after pollination has occurred, and regardless of the oviposition place, they were proved to similarly lay eggs in the most internal ovary layers (West and Herre 1994, Kerdelhu& and Rasplus 1996). Kerdelhue and Rasplus (1996) have suggested that they are unable to oviposit in pollinated ovaries. The other species of non-pollinating fig wasps lay eggs in previously gall-transformed ovaries that already shelter a larva. These insects are either parasitoids (their larva directly feeds on the developing larva of another species) or inquilines (their larva feeds on the gall plant tissue; if the first larva starves to death, the inquiline is functionally parasite; if not, it acts as a commensal). Among dioecious species, Ficus carica is one of the best studied (Valdeyron and Lloyd 1979). Its particular fruiting phonology was proved to stabilize the FicusBlastophaga symbiosis in the south of France. This has led to dioecy being considered as an adaptation to seasonal climates (Kjellberg et al. 1987). Although plausible, this hypothesis is limited by the existence of dioecious figs in tropical environments (Patel et al.

Phenology of Ficus variegata in a seasonal wet tropical forest at Cape Tribulation, Australia

Abstract. We studied the phenology of 198 mature trees of the dioecious fig Ficus variegata Blume (Moraceae) in a seasonally wet tropical rain forest at Cape Tribulation, Australia, from March 1988 to February 1993. Leaf production was highly seasonal and correlated with rainfall. Trees were annually deciduous, with a pronounced leaf drop and a pulse of new growth during the August‐September drought. At the population level, figs were produced continually throughout the study but there were pronounced annual cycles in fig abundance. Figs were least abundant during the early dry period (June‐September) and most abundant from the late dry season (October‐November) through the wet season (December‐April). The annual peak in reproduction actually reflected two staggered peaks arising from gender differences in fig phenology. In this dioecious species, female and male trees initiated their maximal fig crops at different times and flowering was to some extent synchronized within sexes. Fig production in the female (seed‐producing) trees was typically confined to the wet season. Male (wasp‐producing) trees were less synchronized than female trees but reached a peak level of fig production in the months prior to the onset of female fig production. Male trees were also more likely to produce figs continually. Asynchrony among male fig crops during the dry season could maintain the pollinator population under adverse conditions through within‐ and among‐tree wasp transfers.

Pollinators entering female dioecious figs: why commit suicide?

AbstractIn the dioecious fig/pollinator mutualism, the female wasps that pollinate figs on female trees die without reproducing, whereas wasps that pollinate figs on male trees produce offspring. Selection should strongly favour wasps that avoid female figs and enter only male figs. Consequently, fig trees would not be pollinated and fig seed production would ultimately cease, leading to extinction of both wasp and fig. We experimentally presented pollinators in the wild (southern India) with a choice between male and female figs of a dioecious fig species, Ficus hispida L. Our results show that wasps do not systematically discriminate between sexes of F. hispida. We propose four hypotheses to explain why wasp choice has not evolved, and how a mutualism is thus maintained in which all wasps that pollinate female figs have zero fitness.

Evolution of style-length variability in figs and optimization of ovipositor length in their pollinator wasps: A coevolutionary model

Monoecious figs reward their pollinators—agaonid wasps—by allocating a proportion of the flowers for egg laying, and retain the rest for seed production. It has been suggested that these proportions could be regulated by producing short-styled and long-styled flowers such that pollinator wasps could only use the former as their ovipositor does not reach the ovules of the latter. Thus the wasps can lay eggs only in the short-styled flowers and raise their offspring, and the ovules of uninfested, long-styled flowers can develop into seeds. This implied that figs bear dimorphic female flowers, with a bimodal distribution of style length. However, recent studies have shown that style length is distributed normally, with no evidence of bimodality. Therefore the regulation of allocation of flowers to the wasps does not seem to be through the production of two distinct kinds of female flowers. In this article we suggest that two factors govern the proportion of flowers rewarded to the wasps: (i) passive regulation, which is a consequence of the optimization of wasp ovipositor length, and (ii) active regulation, where figs are selected to enhance the variance of style length. We show that these arguments lead to certain predictions about the optimum ovipositor length, the proportion of the flowers available to the wasps, and the coefficient of variation of style length. We also show that data for 18 fig-wasp associations conform well with these predictions. We finally suggest that the regulatory process outlined here can be extended to evolution of style length in dioecious fig species also.

Vicarious selection explains some paradoxes in dioecious fig—pollinator systems

Fig trees (Ficus spp.) are pollinated by small hymenopteran wasps that develop within the fig. In dioecious species, female wasps enter and pollinate `female' figs that produce only seeds and within which the wasp is unable to reproduce. A resolution for three paradoxes in the biology of dioecious fig--pollinator systems is suggested: (i) why wasps enter female flowers, (ii) why they maintain structures and behaviours needed to pollinate female figs, despite the absence of any direct selection on these phenotypes and (iii) why wasps entering male flowers go through the behaviours that would be required to pollinate female figs. Whereas it is obviously in a female fig's interest to conceal her sex from the wasps, it is argued that it is also in a male fig's interest to do so, because the male will benefit only from raising female wasps that, when they leave, successfully find, enter, and pollinate female figs (even though this will be fatal to the wasps).

A mutualism at the edge of its range

Comparing populations that differ in access to mutualists can suggest how traits associated with these interactions have evolved. I discuss geographical and seasonal variation in the success of a primarily tropical mutualism (the fig/pollinator interaction), and evaluate some possible adaptations allowing it to persist at the edge of its range. Pollinators probably have difficulty in seasonal sites because 1) fig trees flower rarely in winter and 2) trees that do flower are less detectable and more difficult to reach. Fig biologists believe that seasonality must have selected for adaptations allowing pollinators to survive winter. However, geographical comparisons do not support two current ideas, the synchrony-breakdown hypothesis and the specificity-breakdown hypothesis. I pose two alternatives: plasticity of fruit and wasp developmental time, and adaptations of free-living fig wasps. I also distinguish between the impact of seasonality on monoecious versus dioecious figs; the latter group appear better adapted to reproduce in cool climates. A combination of comparative, observational, and experimental approaches has great potential for advancing our understanding of mutualisms.

The Stability of the Symbiosis between Dioecious Figs and Their Pollinators: A Study of Ficus carica L. and Blastophaga psenes L.

The Stability of the Symbiosis between Dioecious Figs and Their Pollinators: A Study of Ficus carica L. and Blastophaga psenes L.

THE STABILITY OF THE SYMBIOSIS BETWEEN DIOECIOUS FIGS AND THEIR POLLINATORS: A STUDY OF FICUS CARICA L. AND BLASTOPHAGA PSENES L.

Each Ficus species depends on a specific mutualistic wasp for pollination. The wasp breeds on the fig, each larva destroying a female flower. It is, however, not known why the wasps have not evolved the ability to use all female flowers. In "dioecious" figs, the wasp can only breed in the female flowers of the "male" trees, so that pollination of a female tree is always lethal. The wasps should therefore be selected to avoid female trees. Field data is presented showing that the fruiting phenology of the dioecious fig Ficus carica is such that this selection does not occur: syconia are not receptive at the same time on "male" and female trees. Most wasps are forced to emerge from the syconia of "male" trees at a time when they will not be able to reproduce, whether they avoid female trees or not. This aspect of the life cycle of the wasp, although noticed, has been obscured in most previous studies. It is shown that the fruiting phenology of Ficus carica, which stabilizes the symbiosis, is the result of short-term selective pressures on the male function of the trees. Such selective pressures suggest a possible pathway from monoecy to dioecy in Ficus under seasonal climates.