Fight together or escape? an insect affair!

Fungi specialised to attack insects (in the photo from the blog Hyphal Happenings) are commonly present in the environment so that they have driven many aspects of the insect evolution, affecting behavioural, chemical and immune systems.

In a recent paper published in PLoS One, Christine Turnbull and colleagues compared the activity of cuticular antifungal compounds in thrips species (Insecta: Thysanoptera) representing a gradient of increasing group size and sociality: solitary, communal, social and eusocial, against the entomopathogen Cordyceps bassiana. Solitary and communal species showed little or no activity. In contrast, the social and eusocial species killed this fungus, suggesting that the evolution of sociality has been accompanied by sharp increases in the effectiveness of antifungal compounds. This paper suggests a new insight into the evolution of thrips sociality since traits enabling nascent colonies to defend themselves against microbial pathogens should be considered essential for social evolution. Are fungal entomopathogens an integral part in the evolution of insect sociality in general?

Interestingly, a very different response has been reported by Hatano and colleague in aphids where entomopathogenic fungi stimulate transgenerational wing induction in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae)  allowing aphids to leave patches containing entomopathogenic fungi. Indeed, pea aphids infected with pathogens and maintained in groups on broad bean plants produced a higher proportion of winged morphs than uninfected control aphids.

Wing induction in aphids has been also related to the presence of predators and parasitoids, but unlike predators and parasitoids the effect of  entomopathogenic fungi is independent of physical contact with other aphids, suggesting that physiological cues induce wing formation in infected aphids. Indeed, when maintained in isolation, aphids infected with fungi pathogens also produced higher proportions of winged offspring than control aphids.

As a whole, specialised fungal entomopathogens intensified the degree of sociality and group size in some insects enabling primitive nascent colonies to combat microbial pathogens whereas the same selective agent prompted aphids (that are generally not social insects) to induce wings also in isolated aphids in order to quickly escape infected patches.

Therefore, if you see fungi pathogens fight them with our family or escape them!

References

Turnbull C, Wilson PD, Hoggard S, Gillings M, Palmer C, Smith S, Beattie D, Hussey S, Stow A, Beattie A (2012). Primordial enemies: fungal pathogens in thrips societies. PloS one, 7 (11) PMID: 23185420
Hatano E, Baverstock J, Kunert G, Pel, J, Weisser W. (2012). Entomopathogenic fungi stimulate transgenerational wing induction in pea aphids, Acyrthosiphon pisum (Hemiptera: Aphididae) Ecological Entomology, 37 (1), 75-82 DOI: 10.1111/j.1365-2311.2011.01336.x

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Sex is more attractive than fear… for insects too!

In the last months I found in literature several very intriguing papers about aphids and their biological control. A good example is the paper entitled “Effect of synthetic and plant-extracted aphid pheromones on the behaviour of Aphidius colemani” recently published by O. M. C. C. Ameixa and P. Kindlmann in the Journal of Applied Entomology.

According to this paper the aphid parasitoid Aphidius colemani (in the photo from the Viridaxis homepage) is sensitive to a mixture of odours including both synthetic and plant-extracted nepetalactone (a component of aphid sex pheromone) and (E)-b-farnesene (aphid alarm pheromone). The behavioural responses of A. colemani to three semiochemical groups with different concentrations were studied in a square arena by Ameixa and Kindlmann showing that parasitoid females were significantly attracted by the semiochemicals, when their concentrations were high, in which case the females spent more time in squares with semiochemicals. However, the majority of females preferred plant-extracted nepetalactone, when it was in high concentration, but they consistently did not respond to (E)-b-farnesene.

These results support previous data showing that a high concentration of (E)-b-farnesene became repellent to the egg parasitoid Chrysonotomyia ruforum and that parasitoid females were not attracted by different concentrations of (E)-b-farnesene, but when this component was offered against a background of a non-attractive natural blend of pine volatiles, the combination became attractive… suggesting as a whole that to be detected by the parasitoid, (E)-b-farnesene must be in a combination with other plant volatiles.

As a whole these results are extremely important considering that some trials with genetically modified plants producing (E)-b-farnesene are in progress (as reported here) using (E)-b-farnesene alone making these plants probably not really effective to fight aphids.

Ameixa, O., & Kindlmann, P. (2012). Effect of synthetic and plant-extracted aphid pheromones on the behaviour of Aphidius colemani. Journal of Applied Entomology, 136 (4), 292-301 DOI: 10.1111/j.1439-0418.2011.01638.x

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Sensing aphids

In most aphid species, the volatile sesquiterpene (E)-β-farnesene (Eβf) is released as an alarm pheromone in response to predation and is also emitted continuously at low levels. Some aphid predators use Eβf as a foraging cue, suggesting that the benefits to aphids of signaling via Eβf must be weighed against the cost of increasing apparency to natural enemies.

At the same time, aphid alarm pheromone has been shown to mediate mutualistic interactions between ants and aphids, in which ants protect “myrmecophilic” aphids while collecting aphid honeydew (a rich source of carbohydrates). Nault et al. (1976) observed that ants became very aggressive in the presence of alarm pheromone and increased their rate of attack on aphid predators, but did not attack aphids. In contrast, when alarm pheromone was applied to colonies of aphid species that are not ant-tended (non-myrmecophilic), ants became aggressive towards the aphids themselves (Nault et al., 1976). More recently, ants’ ability to perceive Eβf was confirmed by Mondor and Addicott (2007).

It was frequently believed that ant-aphid mutualisms were tightly linked, coevolved responses. However, it has been proposed that these dyads may evolve, especially in facultative as opposed to obligate mutualists, as ‘loose relationships’ between species explaining why ants are capable of tending multiple aphid species, either simultaneously or sequentially, in their native habitats. The Argentine ant, for example, is capable of tending many different aphid species in its native environment  and many of these aphids are likely to use E-b-farnesene as their alarm pheromone. Interestingly invasive ants, such as Argentine ant in Europe and USA, may form mutualistic associations with native aphids due to selection for this trait in the ant’s native environment.

The study of aphid-ant interaction will be therefore very useful non only to better understand the interaction between these taxa, but also to improve our knowledge about ant invasive species.

(Photo of Alison Bockoven from the blog 6legs2many).

References

• Mondor, E., Addicott, J. (2006) Do exaptations facilitate mutualistic associations between invasive and native species? Biological Invasions, 9 (6), 623-628 DOI: 10.1007/s10530-006-9062-0
• Vandermoten S, Mescher MC, Francis F, Haubruge E, Verheggen FJ (2012) Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. Insect Biochemistry and Molecular Biology, 42, 155-63 PMID: 22178597.
• Verheggen, F., Haubruge, E., De Moraes, C., Mescher, M. (2009) Social environment influences aphid production of alarm pheromone Behavioral Ecology, 20, 283-288 DOI: 10.1093/beheco/arp009

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