Mutualisms, in which individuals of different species help each other, are common. For example, bees pollinate flowers from which they obtain nectar. But some bees take nectar without pollinating and some flowers don’t provide nectar. There are two main ways that a mutualism partner may cheat. First, by not playing its part. Second, by taking too much from the partner. So, what prevents cheating? One possibility is that cheats don’t prosper. Recent research on brood site pollination in figs, in which a female wasp lays its eggs in the some of the fig flowers it pollinates with the wasp larvae eating the seeds, shows that plants can deter cheats. Research on Panamanian figs by Jander & Herre (1) shows that if a female wasp does not pollinate the fig it enters to lay eggs, the plant will often abort the fig thereby punishing non-pollinating wasps. As a result, cheat wasps have fewer offspring than non-cheats which do pollinate. Research on an Asian fig species by Wang et al. (2) investigates cheating by over-exploitation. It seems that the thousands of flowers inside a fig are not all equally easy for the wasps to lay their eggs in, which prevents overexploitation.
The fig ‘fruit’ is actually hundreds of flowers turned in on themselves, so that the plant’s reproductive organs are facing inwards, and protected by the fig structure. The life cycles of fig plants and their co-evolved wasp counterparts are intertwined in an obligate manner, meaning that they need each other in order to reproduce successfully (3).
In narrow seasonal windows, the fig creates a small opening in the bottom of the fruit called an ostiole, which enables female wasps to enter the structure (Fig.1). Only the female fig-wasps have wings, and therefore are able to disperse freely.
Once within the fig, the wasp uses an ovipositor to lay eggs within the ovules of the fig (female gamete, equivalent to animal egg cells). The ostiole then closes so the wasp can’t escape.
During or before egg-laying, the female wasp also carries out another task, of pollinating the flowers she is not laying into. Depending on the species of wasp, this occurs either by passively transmitting pollen through accidental contact when she is laying, or purposefully using forelimbs to unload pollen from specialised thoracic pockets, which will have been filled prior to entering the ostiole.
After the eggs are laid and the female plant structures have been fertilised, the foundress wasp dies. Her wingless male and winged female offspring then hatch (Fig.2), and mate. The males cut holes in the wall of the fig, and the fertilised female wasps pass through the mass of pollen-laden stamen (male sex organ structure of plants), and into the outside world, to find a new fig and repeat the cycle (4).
Through these processes, the relationship between fig and wasp is mutually beneficial, as the wasp’s entire reproductive cycle occurs within the protective structure of the fig, and the fig plant is fertilised, and then new pollen is distributed by the next generation of wasps who disperse. Meaning that the reproduction of each species, and thus continued survival, is dependent on the other (5)
However, mutualistic relationships don’t always run smoothly. Actors within mutualistic relationships are still essentially operating through self-interest, rather than consciously aiming to altruistically help their mutualism partner. Therefore, if there is potential to gain benefit from the other actor, without putting as much effort or time into your side of the interaction, this will be the preferred method, as it is less cost for more benefit.
Fig-wasps have been shown to cheat, by not playing their part and/or by taking too much, through methods such as:
- Foundress wasp not bringing pollen into the fig originally, meaning the flowers do not get fertilised.
- Offspring female wasps not collecting pollen as they leave, meaning they are not spreading the genes of the fig they hatched in.
- Laying eggs in too many ovules, which impacts fig ability to reproduce (ovules are female gametes, pollen is male). Hypothetically, if half of the fig’s ovules get laid into and produce female wasps, and half are fertilised and therefore develop into seeds, this is the perfect ratio. As typically the ideal sex ratio in species is 50:50 male to female, and in this case, and the female wasps are actually acting as the male function for the plant (in most wasp species the sex ratio is not 50:50, because the males are only needed for mating and cutting the females free from the fig (6)).
However, if the foundress wasp lays eggs into over half of the ovules, this disrupts the sex equilibrium, and becomes disadvantageous to the fig.
- Some wasp species have evolutionarily branched off, developing new reproductive methods which are less effort for them; they have developed extremely long and thick specialised ovipositors, which enable implantation into fig ovules without ever entering the fruit (Fig.3) Instead they pierce the fig skin using the reinforced ovipositor, thereby receiving the benefits provided by the fig but contributing nothing to the fig’s reproduction.
In response to these developments by the wasp, figs have evolved deterrent features, to lessen the benefits of the wasp adaptations, thereby discouraging the behaviours. Mechanisms such as a smaller ostiole, shorter ostiole opening periods, quicker fig ripening, as well as the example mentioned in the opening paragraph, are illustrations of evolutionary responses. In a little more detail, the findings of the Jander & Herre study concluded that figs have complex sanctions in place to reduce the ‘fitness’ (survival/ reproductive success) of individuals or species who cheat them. An example of such sanctions from this paper is the abortion/ejection of figs by the plant, if they have been entered by non-pollinating wasps, as there is no benefit to the plant of hosting them (1). This response results in the cheats being killed or prevented from laying their eggs, meaning fewer of them will reproduce and pass on the genes for the cheating behaviour. Therefore, there is an ongoing trade-off between the benefits of not wasting resources on being a good mutualist partner, and the risks of being ‘punished’ by that same partner.
Studies conclude that mechanisms which maintain mutualism equilibrium are not fixed, because they respond directly to the evolving methods of the partner species (2) (1), therefore can be seen as a form of co-evolution, and there is extensive molecular evidence that this ‘cheating’ has evolved multiple times (7).
Despite the interaction between fig plants and fig-wasps being classified as interspecific mutualism (cooperation between two different species), there is still continued evolutionary conflict, as both parties are still driven by self-interest, and will ‘gain’ in the short term by prioritising their needs. Even when cooperating, an evolutionary arms race still occurs, as both parties are working towards different goals.
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2. Discriminative host sanctions in a fig–wasp mutualism. Wang, Rui-Wu. 2014, Ecology , Vol. 95.5, pp. 1384-1393.
3. Figs and fig pollinators: evolutionary conflicts in a coevoled mutualism. Anstett , Marie , Hossaert-McKey, Martine and Kjellberg, Finn. 3, s.l. : Trends in Ecology and Evolution, 1997, Vol. 12.
4. Regulation of seed and pollinator production in the fig-fig wasp mutualism. Nefdt, Rory and Compton, Stephen. s.l. : Journal of Animal Ecology, 1996, pp. 170-182.
5. Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Machando, Carlos, Robbins, Nancy and Herre, Edward . 1, s.l. : Proceedings of the National Academy of Sciences of the USA (PNAS), 2005 , Vol. 102.
6. Optimality, plasticity and selective regime in fig wasp sex ratios. Herre, Edward. 6140, s.l. : Nature, 1987, Vol. 329, pp. 627-692.
7. Conflict, cheats and the persistence of symbioses. Douglas, Angela. 4, s.l. : New Phytologist, 2008, Vol. 177.
8. Britannica, The Editors of Encyclopaedia. Fig Wasp – Insect . Encyclopaedia Britannica. [Online] August 1, 2013. [Cited: March 3, 2020.] https://www.britannica.com/animal/fig-wasp.
9. THE STATUS AND DISTRIBUTION OF FICUS HISPIDA L.f. (MORACEAE) IN SINGAPORE. Lee , Si, et al. 1, s.l. : Nature in Singapore, 2013, Vol. 6, pp. 85-90.
10. Biomechanics of substrate boring by fig wasps. Kundanati , Lakshminath and Gundiah, Namrata. 1, Bangalore : Journal of Experimental Biology , 2014, Vol. 217. 10.1242/jeb.098228.