Make your choice.. of plants!

Aphids harbour several obligate and facultative bacterial symbionts that have important effects on their life. Several surveys of secondary symbionts clearly show that particular species are strongly associated with aphids feeding on certain food plants. For instance, most pea aphid clones feeding on clover Trifolium sp. harbour Regiella insecticola, while those feeding on Medicago usually have Hamiltonella defensa.

How can we explain such a difference? The most intriguing hypothesis is that these patterns reflect a role of these symbionts in the host plant use. However, they may also be present in view of factors correlated with host plant use or simple historical contingency. So the question is: Can symbiont drive the choice of the plant by aphids or they simply change in view of the plants where aphids live?

Several studies tried to distinguish between these explanations furnishing controversial scenarios. Tsuchida et al. (2004) removed R. insecticola from a clover-associated pea aphid clone using antibiotics and found that performance on Trifolium, but not Vicia, was negatively affected. In the same year, Leonardo repeated the same experimental plan but without finding any fitness effects of removing R. insecticola from two clones of aphid specialized on Trifolium. With a different approach, based on the artificial introduction of R. insecticola into five symbiont-free clones not previously associated with clover, no effect on performance of aphids on Trifolium have been observed by Ferrari et al. (2007). These results, as a whole, suggested that symbionts may be involved in the plant choice but not alone. Probably, interactions between aphids and plants involve the genotype of either the host or symbiont and both can influence host plant use.

Ferrari and Godfray here reported a further set of experiments where they evaluated the fitness consequences of introducing different strains of the symbiont Hamiltonella defensa into three aphid clones (that naturally lack symbionts) collected on Lathyrus pratensis and of removing symbionts from 20 natural aphid–bacterial associations. Ferrari and Godfray reported that: “Infection decreased fitness on Lathyrus but not on Vicia faba, a plant on which most pea aphids readily feed. This may explain the unusually low prevalence of symbionts in aphids collected on Lathyrus. There was no effect of presence of symbiont on performance of the aphids on the host plants of the clones from which the H. defensa strains were isolated. Removing the symbiont from natural aphid–bacterial associations led to an average approximate 20 per cent reduction in fecundity, both on the natural host plant and on V. faba, suggesting general rather than plant-species-specific effects of the symbiont. Throughout, we find significant genetic variation among aphid clones”.

Can you have now a better scenario? As a whole, the results provide no evidence that secondary symbionts have a major direct role in facilitating aphid utilization of particular host plant species, but only the aphid genome seem to have a pivotal role in the plant choice. At present we have a reply, but further experiments on different aphid species are welcome!

References

McLean, A., van Asch, M., Ferrari, J., & Godfray, H. (2010). Effects of bacterial secondary symbionts on host plant use in pea aphids Proceedings of the Royal Society B: Biological Sciences, 278 (1706), 760-766 DOI: 10.1098/rspb.2010.1654
Tsuchida, T. (2004). Host Plant Specialization Governed by Facultative Symbiont Science, 303 (5666), 1989-1989 DOI: 10.1126/science.1094611
Leonardo, T. (2004). Removal of a specialization-associated symbiont does not affect aphid fitness Ecology Letters, 7 (6), 461-468 DOI: 10.1111/j.1461-0248.2004.00602.x
Ferrari, J., Scarborough, C., & Godfray, H. (2007). Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids Oecologia, 153 (2), 323-329 DOI: 10.1007/s00442-007-0730-2

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Insects? Not just one genome-one organism

In the last day I read with great interest the intriguing review entitled “A symbiotic view of life: we have never been individuals” written by  Scott F. Gilbert, Jan Sapp and Alfred I. Tauber and published in The Quarterly Review of Biology.

Due to their parthenogenetic reproduction aphids are generally considered a sort of clone so that each individual is identical to the others in the population. According to this suggestion, several Authors refereed to aphids as a single genome species. Actually, as well stated by Gilbert et al, the one-genome/one-organism doctrine of classical genetics has been eclipsed by recent studies on symbiosis. In particular, aphid microbial symbionts form a second type of genome and genetic inheritance (Moran 2007; Gilbert 2011). As frequently suggested, insects may acquire their symbionts vertically though the maternal germline as well as horizontally from the environment (such as during feeding). In particular, in aphids, symbiotic bacteria provide selectable allelic variation (thermotolerance, color, parasitoid resistance) that enables some hosts to persist better under different environmental conditions (Dunbar et al. 2007; Tsuchida et al. 2010).

A well-studied example is the pea aphid, Acyrthosiphon pisum since variants of its symbiont Buchnera provide the aphid with thermotolerance, even if at the expense of fecundity at normal temperatures; Dunbar et al. 2007). The second bacterial symbiont Rickettsiella is responsible for color change, turning genetically red aphids into green through the synthesis of quinones (Tsuchida et al. 2010). Furthermore, variants of Hamiltonella symbionts provide immunity against parasitoid wasp infection (Oliver et al. 2009). Interestingly, in the last case, the protective role of Hamiltonella is due to the incorporation of a specific lysogenic bacteriophage within the bacterial genome. The aphids are therefore infected by Hamiltonella that must be infected by phage APSE-3. As Oliver et al. (2009) wrote, “In our system, the evolutionary interests of phages, bacterial symbionts, and aphids are all aligned against the parasitoid wasp that threatens them all. The phage is implicated in conferring protection to the aphid and thus contributes to the spread and maintenance of H. defensa in natural A. pisum populations” .

However, symbioses are frequently not for free for the hosts and even if aphids have some advantages due to symbionts in the presence of parasitoids having their beneficial protection, in the absence of parasitoid wasps aphids carrying the bacteria with lysogenic phage are not as fecund as those lacking them. Similarly, a trade-off occurs in aphids that carry the thermotolerant genetic variants of Buchnera, meaning that more heat-resistant aphids have less fecundity at milder temperatures than their sisters whose bacteria lack the functional allele for the heat-shock protein.

As Gilber et al reminded at the ned of their review, not all scientists involved in evolution agree about the important role of symbiosis so that, for instance, in the 2009 “Homage to Darwinism” debate held at Oxford University, Richard Dawkins questioned the bringing of symbiosis into evolutionary theory: “Take the standard story for ordinary animals, [where] you’ve got a distribution of animals [and] you’ve got a promontory, or  an  island or something and so you end up with two [geographical] distributions. And then on either side you get different selection pressures, and so one [group] starts to evolve this way, and [the other] one starts to evolve that way, and what’s wrong with that? It’s highly plausible, it’s economical, it’s parsimonious. Why on Earth would you want to drag in symbiogenesis when it’s so unparsimonious and uneconomical?”. As Lynn Margulis replied at that time…  simply because symbiosis exists and it is common in living organisms.

 References

• Dunbar HE, Wilson AC, Ferguson NR, & Moran NA (2007). Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS biology, 5 (5) PMID: 17425405

• Gilbert S. F. 2011. Symbionts as genetic sources of hereditable variation. pp. 283–293. In Transformations of Lamarckism: from sbtle fluids to molecular biology, edited by S. B. Gissis and E. Jablonka. Cambridge (Massachusetts): MIT Press.

• Moran NA (2007). Symbiosis as an adaptive process and source of phenotypic complexity. Proceedings of the National Academy of Sciences of the United States of America, 104 Suppl 1, 8627-33 PMID: 17494762

• Oliver, K., Degnan, P., Hunter, M., & Moran, N. (2009). Bacteriophages Encode Factors Required for Protection in a Symbiotic Mutualism Science, 325 (5943), 992-994 DOI: 10.1126/science.1174463

• Tsuchida T., Koga R., Horikawa M., Tsunoda T., Maoka T., Matsumoto S., Simon J.-C., Fukatsu T. 2010. Symbiotic bacterium modifies aphid body color. Science 330:1102–1104.

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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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