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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Self-damaging wasps.. not stupid, just dirty!

 One of the first twits that I received this morning was from  Discover Magazine and was related to a post entitled “Parasitic wasps vaccinate aphids by spreading anti-wasp bacteria”. Of course the combination of vaccines and aphid is unusual considering that the insect immune system is devoid of memory and vaccination is actually a sort of immune priming rather than a true vaccination.

The interest in this paper is also hampered considering that aphids have a peculiar immune system since, as recently reviewed by Poirié and Coustau (2011), the immune deficiency (IMD) signalling pathway was apparently non functional in aphids and no genes coding for peptidoglycan recognition proteins (PGRPs) and several well-conserved antimicrobial peptides, such as defensins and cecropins, have been predicted in the pea aphid Acyrthosiphon pisum.

Actually the authors of the paper entitled “Parasitoids as vectors of facultative bacterial endosymbionts in aphids” do not refer to vaccination, even if they described a very intriguing event due to parasitoids! An example is Aphidius colemani showed in the Jarmo Holopainen photo from PBase.

Gehrer and Vorburger demonstrated ”that parasitoids can transfer endosymbionts of Aphis fabae aphids between clones by sequentially stabbing infected and uninfected aphids—a previously undescribed route of horizontal transmission. The wasp’s ovipositor appears to act as a ‘dirty needle’ that can inoculate previously uninfected aphids. If the recipient aphid resists the parasitoid and survives the attack, this can result in a new, heritable infection. Considering the fact that many aphid parasitoids use multiple hosts, it is likely that they can transfer endosymbionts not just within but also between aphid species.”

But that’s not all… the two bacterial symbionts that have been transferred by wasps are Hamiltonella defensa and Regiella insecticola and both have a protective function in aphids. Indeed, the first is known to increase aphid resistance to parasitoids whereas the latter  protect aphids against fungal pathogens. The wasp-mediated transfer of H. defensa is very intriguing from an evolutionary point of view since wasps are spreading a symbiont (H. defensa), which provides aphids with protection against parasitoids (including wasps), so that wasp-mediated transfer is detrimental to their own fitness. This result could seem strange or self-damaging, but actually, as perfectly exemplified by Gehrer and Vorburger, wasps are simply using ‘dirty needles’ so that they are not self-damaging but just paying a price for their dirty work!

Gehrer, L., & Vorburger, C. (2012). Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biology Letters DOI: 10.1098/rsbl.2012.0144

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Aphids and their ecological immunity

Bacteria commonly interact with aphids in intimate symbioses, where symbionts increase host fitness (for a review see Russell and Moran, 2006). Interestingly, several evidences suggested that symbiotic bacteria present in the insect gut are involved not only in the degradation of specific substances in the food (Russell and Moran, 2006), but also in other complex interactions protecting the host from invasion by pathogenic microorganisms (a process known as “colonization resistance”) and modulating the insect immune system. Microbiome seems therefore to act in aphids (and actually not only in insects) as a sort of ecological immunity or extended immune system being able of affecting the efficiency of the host immune system and limiting the accumulation of pathobionts. As evident in the photo from a Nancy Moran paper, aphid bacteriocytes possess several symbiotic bacteria including the larger Buchnera primary symbionts (arrowheads) and the smaller H. defensa secondary symbionts (arrows).

In a recent paper, Chiu et al. (2012) reported a low survival of nymphs of the aphid Myzus varians at high temperatures as a consequence of the elimination of endosymbionts, such as Buchnera. This effect probably results from a temperature-mediated decrease in aphid endosymbionts, which synthesize amino acids essential for their insect hosts. In the last years, different roles have been suggested for symbionts other than the synthesis of amino acids only (Russell and Moran, 2006). Buchnera might, for instance, play a key role in aphid thermal tolerance since endosymbionts code for heat shock proteins, which deter degradation of host protein secondary structure (Dunbar et al., 2007). Secondary endosymbionts, such as Serratia simbiotica, play a similar role in the thermal tolerance of their host strengthening the ability of aphids to evolve further adaptations to overcome the impacts of warming (Russell and Moran, 2006).

Buchnera are at least partly able to survive at high temperatures because of constitutive expression of genes that are normally up-regulated in response to heat and aphids could be able to thrive under temperatures as high as 35°C in the laboratory (Dunbar et al., 2007). Surprisingly, a single nucleotide deletion in the Buchnera ibpA gene encoding for a small heat-shock protein virtually eliminates the transcriptional response of ibpA to heat stress and lowers its expression even at cool or moderate temperatures (Dunbar et al., 2007). In the present of this mutant allele, a short heat exposure in juveniles has strong effects on aphids that produce few or no progeny and contain almost no Buchnera, in contrast to aphids bearing symbionts without the deletion.

The ibpA mutated allele has appreciable frequencies in field populations supporting the view that lowering of ibpA expression improves host fitness under some conditions (Dunbar et al., 2007). As previously suggested, the response to stress (including thermal stress) is part of a large trade-off that related stress response to reproduction and immunity. This mutation by switching off the response to heat stimuli could favor aphid reproduction and immunity. However, the prolonged permanence of aphids at high temperatures (for instance in hot summer with daily mean temperature of 32.5 °C) results in the elimination of Buchnera reducing not only the thermal tolerance of aphids, but also their fecundity since the lack of endosymbionts results in a lost synthesis of amino acids essential for the hosts (Chiu et al., 2012).

According to these results, global warming could be difficultly faced by aphids in tropical regions due to Buchnera symbiont depletion.  Interestingly, in the presence of low density of primary symbionts, secondary symbionts (such as Hamiltonella defensa,  Serratia symbiotica, Regiella insecticola) could be more present affecting not only the aphid thermal tolerance to high temperatures clearly suggesting, but also their immune response due to symbionts (Poirié and Coustau, 2011).

The effects of global warming on the composition of aphid microbiota are of particular interest since, as recently reviewed by Poirié and Coustau (2011), the immune deficiency (IMD) signalling pathway was apparently non functional in aphids and no genes coding for peptidoglycan recognition proteins (PGRPs) and several well-conserved antimicrobial peptides, such as defensins and cecropins, have been predicted in the pea aphid Acyrthosiphon pisum genome (Gerardo et al., 2010), making the microbiota-based immunity essential to protect the host against natural enemies (Poirié and Coustau, 2011).

Even if effective, the symbiont-associated immunity appears to be more ephemeral and less stable than genetic resistance (Poirié and Coustau, 2011). Indeed, the rate of vertical transmission of symbionts is not always 100 %, so that bacteria can be lost, and their presence seems to be more energetically costly (Poirié and Coustau, 2011).

References

Chiu, M., Chen, Y., & Kuo, M. (2012). The effect of experimental warming on a low-latitude aphid, Myzus varians Entomologia Experimentalis et Applicata, 142 (3), 216-222 DOI: 10.1111/j.1570-7458.2011.01213.x

Dunbar, H.E., Wilson, A.C., Ferguson, N.R. & Moran, N.A. (2007). Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS biology, 5 (5) PMID: 17425405

Poirié, M. & Coustau, C. (2011). The evolutionary ecology of aphids’ immunity. Inv. Surv. J., 8, 247-255

Russell, J.A & Moran, N.A. (2006). Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings. Biological sciences / The Royal Society, 273 (1586), 603-10 PMID: 16537132

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