Interactions Between Figs and Gall-Inducing Fig Wasps: Adaptations, Constraints, and Unanswered Questions

The ancient interaction between figs (Ficus, Moraceae) and their pollinating fig wasps is an unusual example of a mutualism between plants and gall-inducing insects. This review intends to offer fresh perspectives into the relationship between figs and the diversity of gall-inducing sycophiles which inhabit their enclosed globular inflorescences that function as microcosms. Besides gall-inducing pollinators, fig inflorescences are also inhabited by other gall-inducing wasps. This review evaluates the state of current knowledge on gall-induction by fig wasps and exposes the many lacunae in this area. This review makes connections between fig and gall-inducing wasp traits, and suggests relatively unexplored research avenues. This manuscript calls for an integrated approach that incorporates such diverse fields as life-history theory, plant mate choice, wasp sexual selection and local mate competition, plant embryology as well as seed and fruit dispersal. It calls for collaboration between researchers such as plant developmental biologists, insect physiologists, chemical ecologists and sensory biologists to jointly solve the many valuable questions that can be addressed in community ecology, co-evolution and species interaction biology using the fig inflorescence microcosm, that is inhabited by gall-inducing mutualistic and parasitic wasps, as a model system.

A solution to a sex ratio puzzle in Melittobia wasps

The puzzling sex ratio behavior of Melittobia wasps has long posed one of the greatest questions in the field of sex allocation. Laboratory experiments have found that, in contrast to the predictions of theory and the behavior of numerous other organisms, Melittobia females do not produce fewer female-biased offspring sex ratios when more females lay eggs on a patch. We solve this puzzle by showing that, in nature, females of Melittobia australica have a sophisticated sex ratio behavior, in which their strategy also depends on whether they have dispersed from the patch where they emerged. When females have not dispersed, they lay eggs with close relatives, which keeps local mate competition high even with multiple females, and therefore, they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they interact with nonrelatives, and thus adjust their sex ratio depending on the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.

Solving the sex ratio scandal in Melittobia wasps

The scandalous sex ratio behaviour of Melittobia wasps has long posed one of the greatest problems for the field of sex allocation. In contrast to the predictions of theory, and the behaviour of numerous other organisms, laboratory experiments have found that Melittobia females do not produce less female-biased offspring sex ratios when more females lay eggs on a patch. We resolve this scandal, by showing that, in nature, females of M. australica have sophisticated sex ratio behaviour, where their strategy also depends upon whether they have dispersed from the patch where they emerged. When females have not dispersed, they will be laying eggs with close relatives, which keeps local mate competition high, even with multiple females, and so they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they will be interacting with non-relatives, and so they adjust their sex ratio depending upon the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness, and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.

The efficacy of natural selection in producing optimal sex ratio adjustments in a fig wasp species

Ever since Darwin's discovery of natural selection, we expect traits to evolve to increase organisms' fitness. As a result, we can use optimization models to make a priori predictions of phenotypic variation, even when selection is frequency-dependent. A notable example is the prediction of female-biased sex ratios resulting from local mate competition (LMC) and inbreeding. LMC models incorporate the effects of LMC and inbreeding. Fig wasp sex ratio adjustments fit LMC predictions well. However, the appropriateness of LMC models to fig wasps has been questioned, and the role that a coincidental by-product plays in creating the apparent fit has been clearly illustrated. Here, we show that the sex ratio adjustments of a fig wasp are the result of a dual mechanism. It consists of a standard facultative LMC response favoured by natural selection, as well as a mechanism that may be the result of selection, but that could also be a coincidental by-product. If it is a by-product, the fitness increase is coincidental and natural selection's role was limited to fine-tuning it for higher fitness returns. We further document a case of an apparent fitness-reducing sex ratio adjustment. We conclude that the use of the adaptationist approach demands that our understanding of traits must be remodelled continually to rectify spurious assumptions.