The Myterious Maintenance of Mutualisms
There are countless examples of mutualisms in nature, yet their ability to persist is somewhat perplexing. Various plant–insect pollinator mutualisms have been studied in detail in order to gain an insight into this weird and wonderful topic, with particular focus on the underlying mechanisms, such as sanctions, maintaining these close relationships.
Around 80% of all flowering plant species are pollinated by animals, insects, vertebrates and mammals – but the main pollinators are insects [1]. This astounding figure reflects the widespread existence of plant-insect pollinator mutualisms. These are tightly woven relationships between a plant and an insect which result in net costs and benefits for both participants [2]. Mutualisms have evolved numerous times across many different taxa and involve reciprocal exploitation. They are extremely important in both an environmental and economic sense. In fact, pollinators affect 35% of the world’s crop production [1]. Furthermore, partners of a mutualism influence the population size and genetic diversity of one another [3].
Explaining the persistence of mutualisms is challenging because at a glance they often appear to be evolutionarily unstable. In order for mutualisms to be advantageous for each partner species, benefits from the relationship (ultimately in the form of reproductive gain) need to outweigh the costs. However, there are ways in which the benefit-cost balance can change, resulting in a potentially unstable mutualism. For example, it would be logical for one partner in a mutualistic relationship to find a way of avoiding any costs at all. However, if a partner achived this, the cost suffered by the other species in the partnership would increase and the benefit to that species would decrease. This would make remaining in the mutualism counterintuitive.
'Cheaters', who completely avoid mutualism costs, do exist in nature and will outcompete any individuals who are ‘non-cheaters’ within their population because they are ultimately fitter [3]. Therefore, ‘cheating’ types can quickly spread. An example of cheating is when bumble bees rob Ipomopsis aggregata flowers of nectar by biting a hole in the corolla. This act allows the bees to acquire their food without touching the pollen rich anthers. The plant then suffers from lack of pollination as well as nectar loss and so its fitness is reduced along with the overall benefit it receives from the mutualism. Thus, plants that suffer from nectar robbing must defensively adapt to prevent fitness loss if the mutualism is to be maintained.
The fig tree-fig wasp mutualism is also subject to cheating pollinators. Jandér & Herre explored this mutualism, focusing specifically on monoecious figs which house both male and female flowers [4]. Some fig wasp species purposely pollinate the flowers within a fig and are consequently called active pollinators. The females of these wasp species lay their eggs in the ovaries of female flowers in just one fig and at the same time they pollinate the male flowers with pollen carried from their natal fig [4]. In this way the fig tree benefits from the mutualism by being pollinated at the expense of the fig wasp’s time and energy, but it loses potential seeds to the wasp’s offspring. Not only does the fig provide food but it also supplies a safe haven in which the young wasps can develop [4]. However, the benefits the fig tree receives from this relationship outweigh the costs, making any losses justifiable.
Some active pollinator insect species cheat by laying eggs in a fig without pollinating the flowers. This fig would yield hardly any seeds, making the cost to the fig tree larger than the benefit of the mutualism. In response to pollinator cheating, fig trees implement selective abortion whereby they abscise unpollinated figs to conserve resources. In this way fig wasps are forced to cooperate and pollinate the fig tree flowers in order to reduce their offspring mortality [4]. The fig tree-fig wasp mutualism would also break down if the wasps were to lay too many eggs in the figs and so destroy a great number of seeds. Preventing this problem is yet again the mechanism of selective abortion, whereby a fig is aborted if the number of eggs within it is above a certain threshold [4].
As with the fig tree-fig wasp mutualism, Goto et al. found that selective abortion prevents the laying of too many eggs in Glochidion flowers which are pollinated by Epicephala moths [2]. The probability of abortion increases with egg load and ovule damage. In this way, selective abortion reduces the immediate degree of overexploitation by moths and also restricts the population size of moths, which in turn reduces the chance future overexploitation. This mechanism stabilises the mutualism, as does the avoidance of pre-infested flowers by Epicephala moths [2].
There are a few important points to note when considering how these acts of mutualism reinforcement came about. Firstly, the ability of Epicephala moths to avoid preinfested flowers did not necessarily evolve as an adaptation to selective abortion - instead it could be down to resource limited competition, as is true for the egg distribution of various Lepidopteran taxa [5]. Selective abortion itself did not evolve solely as a pollinator control for plant-pollinator mutualisms. The abortion of unpollinated flowers, in order to conserve resources, is a relatively common occurrence within and outside of mutualisms [4]. Additionally, abortion may not be directly due to the laying of an a significantly damaging number of eggs but more generally due to insect damage. Many Yucca plant species express this trait [6].
Selective abortion is not the only method used to reduce ‘cheating’ within the aforementioned mutualisms. The Glochidion tree also produces a large number of excess female flowers which are thought to act as sinks for Epicephala moth eggs. Furthermore, figs containing unpollinated flowers and wasp eggs may not be abscised but instead wasp offspring survival is somehow reduced through another mechanism [7]. This last point is likely to be because of decreased food (seed) availability for wasp offspring and poorer gall formation around the young [8].
In conclusion, plant-insect pollinator mutualisms are maintained by underlying mechanisms such as sanctions enforced by the host plant [7]. These underlying mechanisms did not necessarily directly evolve in response to cheating but nonetheless maintain cooperation. One such example of a sanction is selective abortion which appears to have developed from the pre-existing trait of preventing wastage of resources through carrying unpollinated flowers. The selective abortion sanction can prevent ‘cheaters’ from becoming common within a population, as seen with the fig tree-fig wasp, and Glochidion tree and Epicephala moth mutualisms, maintaining the cost-benefit balance within a mutualism [2], [4]. Without these sanctions and other underlying mechanisms, such as the production of excess flowers by the Glochidion tree, it is likely that plant- insect pollinator mutualisms would become unjustifiable due to an unbalanced cost-benefit ratio and so eventually fail.
Photograph: By Ch'ien Lee [CC-BY-2.5 (http://creativecommons.org/licenses/by/2.5)], via Wikimedia Commons
Food and Agriculture Organization of the United Nations, (2011), Pollinators. [online] Available at: http://www.fao.org/biodiversity/components/pollinators/en/ [Accessed 28th February 2012]
[2] Goto R., Okamoto T., Kiers, T. E., Kawakita A. & Kato M., (2010), Selective flower abortion maintains moth cooperation in a newly discovered pollination mutualism, Ecology Letters, 13: 321-329.
[3] Kearns C. A., Inouye D. W. & Waser N. K., (1998), Endangered mutualisms: the conservation of plant-pollinator interactions, Annual Review of Ecology and Systematics, 29: 83-112.
[4] Jandér C. K. & Herre E. A., (2010), Host sanction and pollinator cheating in the fig-tree wasp mutualism, Proceedings of the Royal Society of Biology, 277: 1481-1488.
[5] Thompson J. N. & Pellmyr O., (1991), Evolution of oviposition behaviour and host preference in Lepidoptera, Annual Review of Entomology, 36: 65-89.
[6] Pellmyr O. (1997), Stability of plant–animal mutualisms: keeping the benefactors at bay, Trends Plant Science, 2: 408–409.
[7] Herre E. A., Jandér C. K. & Machado C. A., (2008), Evolutionary Ecology of Figs and Their Associates: Recent Progress and Outstanding Puzzles, Annual Review of Ecology, Evolution and Systematics, 39: 439-50.
[8] Jousselin E., Hossaert-McKey M., Herre E. A. & Kjellberg F., (2003), Why do fig wasps actively pollinate monoecious figs?, Oecologia, 134(3): 381-387.
