Cheaters in Mutualisms

Ants are involved in an astounding diversity of symbiotic relationships: they pollinate flowers, they disperse seeds, they farm fungi, they defend trees and insects from natural enemies, etc. Those are some very diverse services! But of course, even when the ants are dutifully performing those services, the ants don’t necessarily benefit their partners. For instance, ants may also sterilize their host plants or eat some of the aphids that they are tending for honeydew. Furthermore, the net outcome for the ants’ partners may be context specific, where the costs and benefits of interacting with ants vary with ecological and environmental conditions. For instance, if you’re an Acacia tree, having ants around to protect you from elephants may be very beneficial, but only if you live in an area that actually has elephants.

Here’s a different question: do ants always benefit from their relationships with their partners? Ants appear to be the decision makers in many of these relationships, where trees and aphids and scale insects and fungi seem less capable of making active decisions to participate (or not) in the relationship. But it turns out that ant partners aren’t as passive as they seem, because they can often use “rewards” and/or “sanctions” to control ants. For example, trees can ‘decide’ how many domatia to produce or whether to produce extrafloral nectar, which in turn determines whether ants will be attracted to the tree. (For an example of a cool sanction, check out this system, where hosts eat their symbionts when the symbionts aren’t beneficial!)

Ants can also experience negative effects of symbiotic interactions when they are tricked by mimic species or individuals called “cheaters.” In fact, there are many neat insect species that trick ants. I really want to go crazy and devote a six page blog post to all of my favorite ones, but here are just two:

1) The lacewing larva that wears aphids: Yes, for real. Lacewing larvae eat aphids, but that can be hard to do when the aphids are protected by ants. So, these lacewing larvae have evolved to wear aphid carcasses (or the cottony-fluff that aphids create) like the proverbial sheep suit worn by the wolf. The ant defenders can’t detect the difference between the aphids and the lacewings in aphid clothing, so the lacewings get to sneak onto the aphid farm to feast without being chased off.

2) Aphids that aggressively mimic ants: A single species of aphid can often have several distinct phenotypes. For instance, there are phenotypes with wings that disperse across relatively long distances and wingless phenotypes that don’t disperse very far. In some aphid species, there are phenotypes that reproduce, and other soldier phenotypes that never reproduce and protect the colony from natural enemies. Finally, in the species Paracletus cimiciformis, there is a green, pot-bellied aphid phenotype that has a typical symbiotic relationship with ants, where the ants protect and clean the root-dwelling aphids in return for honeydew. There is also a second phenotype that is flatter and yellow-ish, with hydrocarbons in the cuticle that are similar to the hydrocarbons in ant larvae (Salazar et al. 2015). When adult ants find aphids with the flat phenotype, the ants carry the aphids back to the ant nest, and plop the aphids onto the piles of ant larvae. From there, the aphids feed on the hemolymph of the ant larvae using their piercing/sucking mouthparts! So, the aphids get to hang out in the protective environment provided by the ant nest while sucking on baby ant juices, and they don’t have to do anything in return. Awesome.

References:

Salazar, A., B. Furstenaub, C. Quero, N. Perez-Hidalgo, P. Carazo, E. Font, D. Mantinez-Torres. 2015. Aggressive mimicry coexists with mutualism in an aphid. PNAS 112(4): 1101-1106.

How beneficial are defensive symbionts?

(This post is late. Sorry, Folks! In my defense… snail dissection. So. much. snail. dissection.)

In my aphid cartoons thus far, Sal the Aphid has been bragging about how she has H. defensa. But just how awesome is it to harbor defensive bacteria? Like we said last time, when aphids get attacked by parasitoid wasps, aphids with H. defensa are more likely to survive than aphids without H. defensa. That seems like a pretty big bonus provided by the symbionts. We might expect natural selection to then favor aphid lineages with symbionts, leading to domination by lineages with H. defensa. But that isn’t what we see. Instead, only some aphids have H. defensa – the symbionts are maintained at intermediate frequencies. So, if defensive symbionts are so great, then why don’t all aphids have them?

In some earlier work, researchers found that H. defensa may not always be beneficial for aphids. For instance, when no parasitoids are present, the frequency of H. defensa in aphid populations declines, suggesting that H. defensa may be costly to maintain (Oliver et al. 2008). So, Vorburger et al. (2013) set out to determine whether the cost of harboring H. defensa is constitutive, induced, or both. That is, is H. defensa always costly, regardless of parasitoid presence (constitutive cost), does the cost come after a parasitoids attack and H. defensa kill the parasitoid larvae (induced cost), or both?

To test this question, Vorburger et al. (2013) exposed aphids with and without H. defensa to attacks by parasitoid wasps. The first 2/3 of the aphids that the wasps attacked were put in an “attacked” treatment group, and the aphids that the wasps did not attack were put in an “unattacked” treatment group. And then Vorburger et al. (2013) kept track of aphid survival and reproductive output.

Like we said last time, when aphids had H. defensa, they were more likely to survive a wasp attack. But when aphids weren’t attacked by wasps, the aphids with H. defensa had reduced fitness in comparison to aphids without H. defensa. That’s the constitutive cost we mentioned before. For aphids without H. defensa, attacked aphids had lower lifetime reproduction than unattacked aphids. That makes sense, of course. But get this: for aphids with H. defensa, attacked aphids had higher lifetime reproduction than unattacked aphids. That’s the opposite of an induced cost! It’s an induced benefit!

So, what caused the “induced benefit”? Well, Vorburger et al. (2013) aren’t sure. But they have one amazing hypothesis. They suggest that maybe when a wasp injects all that venom into an aphid, it kills off a bunch of the H. defensa. That is, the induced benefit is to reduce the constitutive cost of harboring H. defensa by killing off some of those costly symbionts. In that case, H. defensa isn’t sounding so nice afterall, is it? 

I rest my case: parasites and parasitoids are crazy awesome.

Oh, and the paper is open access! Check it out!

Reference:

Oliver, K.M., J. Campos, N.A. Moran, and M.S. Hunter. 2008. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. B Biol. Sci. 275:293–299.

Vorburger, C., P. Ganesanandamoorthy, and M. Kwiatkowski1. 2013. Comparing constitutive and induced costs of symbiont conferred resistance to parasitoids in aphids. Ecology and Evolution 3(3):706-13.

Defended Hosts are Frassheads

Last week, I told you guys that parasitoid wasps respond to H. defensa, which is a bacterial endosymbiont that protects aphids from wasps.  Next week, I’m going to talk about how H. defensa affects aphid fitness.  But first, what is the magnitude of the protective effect?  Well, it varies with the strain of H. defensa and the aphid species and probably lots of other factors, too.  But in the example that I’m going to discuss next week, aphids without H. defensa have a 38% probability of becoming mummies if they get attacked by wasps, while aphids with H. defensa only have a 4% chance of becoming mummies if they get attacked by wasps (Vorburger et al. 2013).  So, H. defensa reduces the probability of mortality after attack by 89.5%!

 

Stay tuned to see what happens to Sal and Lisa.  Are they up Frass Creek without a paddle?

Reference:

Vorburger, C., P. Ganesanandamoorthy, and M. Kwiatkowski. 2013. Comparing constitutive and induced costs of symbiont conferred resistance to parasitoids in aphids. Ecology and Evolution 3(3):706-13.

 

How do parasitoids respond to defended hosts?

Last week, I talked about the new Godzilla movie and how I thought that the MUTOs should have been parasitoids.  This week, let’s talk about some awesome, real life parasitoids: parasitoid wasps (Aphidius ervi).

Quickly, the life cycle works like this: the female wasp finds an aphid nymph, she stabs the aphid with her ovipositor, and then she typically lays one egg inside the aphid.  After one day, the egg hatches into a larval parasitoid, and the larva hangs out inside the aphid while eating the aphid’s innards.  After about one week of this, the aphid dies.  Actually, the aphid’s corpse becomes a “mummy,” and the larva pupates inside the mummy before eventually emerging as an adult parasitoid.  Mating happens, and then the female wasps go off to infect more aphids.

But here’s an interesting complication: some aphids are protected by bacterial symbionts (Hamiltonella defensa).  The degree to which aphids are protected varies with the strain of H. defensa, but the take-home message is that when a wasp lays an egg inside an aphid, the egg is much less likely to survive to adulthood if the aphid has H. defensa symbionts (Oliver et al. 2012).  However, if a wasp lays two eggs inside an aphid with H. defensa symbionts – which is not what wasps usually do – then one larva is more likely to survive than it would have been if it had been a single egg.  In other words, only one larva is going to make it out of there alive, even when two eggs are laid, but one of the larvae is better off than it would have been if it were a single egg.

You might be thinking, “Why, what an interesting tidbit.  Who cares?”  NATURAL SELECTION CARES.  Just kidding, natural selection isn’t sentient, but natural selection should favor any wasp strategies that increase wasp fitness.  And wasp fitness is higher when more wasp eggies turn into wasp larvae and then adult wasps.  And wasp larvae are less likely to die in aphids with H. defensa if two eggs are laid in the aphid, instead of the typical single egg.  See where I’m going with this?

Yes, wasps can differentiate between aphids with and without H. defensa.  And when aphids have H. defensa, wasps are much more likely to lay two eggs in those defended aphids than they are to lay two eggs in undefended aphids.  And that, my friends, is amazing.  While wasps still probably have reduced fitness when infecting defended aphids, the superinfecting tactic (=laying two eggs) likely compensates for some of the reduced fitness.

 

(Yes, sometimes aphids have conversations in my head, and I write them down. You’re welcome.)

Check out the open access paper to learn about the mechanism behind the success of superinfection:

Reference:

Oliver, K.M., K. Noge, E.M. Huang, J.M. Campos, J.X. Becerra, and M.S. Hunter. 2012. Parasitic wasp responses to symbiont-based defense in aphids. BMC Biology 10:11.