I’ve posted a lot about morphological mimicry in animals: the evolved resemblance of one species’ appearance to that of another, or to the environmental background. This mimicry can serve to protect animals from being spotted by predators, or, if you’re a predator, to hide yourself from your prey.
The latter situation, in which animals resemble something else so they can kill or injure members of another species, is called aggressive mimicry. And an intriguing new example of this is reported in a paper in The Proceedings of the National Academy of Sciences by Adrián Salazar and six colleagues (free download, reference below). The mimicry, however, involves chemistry rather than appearance. In the new case, an aphid has evolved to secrete the hydrocarbons that are on the surface of larvae of an ant with which the aphid is normally associated. This mimicry deceives the ants, who can’t see very well but are sensitive to chemical signals. The ants then carry the aphids into the nest and deposit them in the brood chamber, whereupon the duplicitous aphids pierce the larvae with their mouthparts and suck out the hemolymph.
The story is actually quite complex, so I’ll leave out a lot. The aphid, Paracletus cimiformis, is found mostly in Europe but also in Asia and North Africa. It lives on the roots of plants, and, to make matters complicated, is associated with several species of ants. The one studied by the authors is Tetramorium semilaeve, common in Spain, where the research took place. Further, the life cycle of the aphid, as with most aphids, is very complicated, as it successively alternates between two plants hosts, the turpentine tree and grasses. On top of that, the aphids can exist as either winged or wingless forms, and as both sexual and asexual forms. The asexual ones reproduce parthenogentically: unfertilized but diploid eggs (produced without the normal meiotic cell division) are produced by the mother, kept inside her body, and then the young aphids are born alive. The offspring are thus clones of the mother.
Finally—and most important for our purposes—the aphids have two interesting features. The first is that the adults on the grasses (their “secondary” host) come in two forms, a flat whitish form (I’ll call it “flat”) and a more rounded, olive-green form (I’ll call it “round”). These differences are apparently not genetic: white aphids can produce green offspring and vice versa, probably depending on the environmental conditions experienced by the parent and offspring. (Note, though, that the program permitting such switches is undoubtedly coded in the aphid’s genes.)
And those two forms do different things. The round green aphid is a mutualist with the ant: it is trophibiotic, which means in this case that the aphids, after sucking the plant sap, secrete honeydew out of their butts, and the ants eat it. In return, the ants provide the aphids with protection from predators. This is thus a mutualism, a behavior of a pair of species in which both benefit from their relationship (a famous example are lichens, which are actually mixtures of algae and fungi that help each other).
The flat aphid is the one that chemically mimics the ants’ brood, gets carried into the nest, and sucks the hemolymph (insect “blood”) out of the ant larvae. (It’s not yet clear whether the ant larvae are actually killed or just donate a bit of blood, but the researchers did find ant DNA in the flat aphids, and watched them attack the larvae.) That is regarded as aggressive mimicry, and can be seen as either parasitism or predation on the ants. So the aphids have a complex mixture of wingedness and winglessness, sexual and asexual reproduction, living on either trees or grasses, and forming either mutualistic round forms or predatory white forms. (These forms are called “morphs”.) This diagram below shows the complexity; I’ve added the caption from the paper as well. You can ignore all of this except for the round and flat forms on the right:
Below is a photo of the ants and aphids. Panel A shows the ants waving their antennae at the round green form, which is a signal for the aphids to excrete honeydew for the ants to eat. Observations show that waving occurs only with the round form, followed by antennal tapping of the aphid’s butt when it excretes honeydew. The flat aphids are never waved at by ants, but only tapped, a behavior called “antennation.”
Panel B shows the flat white aphids in the brood chamber among the ant larvae (arrows show the aphids, which resemble the brood). Panel C shows the white form sinking its rostrum (the sucking apparatus) into a juicy ant larva, getting ready to suck out the larval hemolymph. Panel D shows a larva leaking hemolymph (the bubble) after being attacked:
The authors tested the hypothesis that the flat white aphids had something about them besides appearance that deceived the ants into thinking they were brood (it wasn’t appearance, for the flat and round aphids are treated differently even in complete darkness). The obvious hypothesis is “chemical mimicry.” So they first showed, using gas chromatography, that the hydrocarbon profile of the flat white aphids was more similar to that of the ant larvae than to the profile of round green aphids.
Virtually all insects have a layer of hydrocarbons on their cuticle; these normally act to prevent desiccation and also act as chemical signals. I worked on this in Drosophila for several years, and showed that different species discriminate against each other when the males “taste”—using chemoreceptors on their forelegs—the hydrocarbons on the females prior to mating. And you can change that discrimination by transferring hydrocarbons between females of different species, something I discovered you can do by simply crowding a female of one species with a gazillion females of another. (I called this the “Tokyo subway experiment”.) The “target” female gets a lot of the foreign hydrocarbons rubbed off onto her body, which affects how males court her.
First, here are the hydrocarbon profiles (a readout from a gas chromatrograph) of the two forms of aphids and the ant larvae. An analysis of the composition (the cuticle contains many hydrocarbons) shows that the flat aphid is more similar to the ant larva than either is to the round aphid, something shown on the right. The differences between aphid morphs isn’t simply due to their acquiring hydrocarbons from ant larvae by contact, for the differences persist when aphids are raised in the lab without any contact with ants.
Finally, the authors tested whether the hydrocarbon differences had any significance for the ants’ behavior. They did. This experiment was done simply by impregnating dummy aphids with extract from either ant larvae, flat aphids, round aphids, or the hexane solvent used to extract hydrocarbons (the control). Ants not only tapped the dummies more when they were impregnated with ant-larval or flat-aphid extract than with round-aphid extract, but only the dummies impregnated with round-aphid extract were waved at. Further, only the dummies impregnated with ant-larval or flat-aphid extract were carried into the nest; this never happened with control dummies or those carrying round-aphid extract. (There are some problems with the statistical significance of these behaviors, so the results are more suggestive than definitive.)
The chemical profiles, as well as the ants’ behavior, suggest that the flat morph has evolved to deceive the ants. This appears to be a derived condition, for all the related aphids we know about have only the mutualistic and round honeydew-excreting form.
This raises several questions. I’ll mention only two. First, how did this evolve? Although the flat and round forms are apparently genetically similar, with the difference controlled by some environmental cue (which cue is another question), the genetic program that causes an aphid to become either round or flat is in the aphids’ genome, a program triggered in one direction or another by environmental cues. The program and environment-sensitive switch are certainly the product of natural selection. But how the flat form evolved from the white form, while both continue to coexist, is a mystery, and we don’t know a lot about how other aspects of aphids’ complex life cycle evolved. There are multiple genetic programs in this aphid (flat vs. round, sexual vs. asexual, winged vs. wingless, tree-dwelling vs. grass-dwelling), and it boggles the mind to consider how they could have evolved. (I suppose the Discovery Institute will use our ignorance to cry “God designed it!”)
Second, what keeps both forms of aphid present in a single population? One obvious answer is a kind of “frequency-dependent selection”. That is, although the differences between flat and round are based on environmental cues, the genetic program has probably evolved to respond to those cues in an adaptive manner, producing different forms when they are most adaptive. One theory, which is mine, is that when the flat forms get too numerous, the round ones have an advantage because the ants’ brood will be diminished so severely that the colony may go extinct, endangering the survival of all aphids associated with the colony. This becomes more probable when many aphids are clones, because selection on one is selection to precisely the same degree on clone-mates.
Conversely, when there are lots of round aphids, there may be an advantage to avoiding competition by producing the flat form that occupies a completely different feeding niche.
These advantages depend on the relative frequency of the two forms, which is why it’s called frequency-dependent selection. (This is selection operating not on the genetic program that codes for the two different appearances and behaviors, but on the genetic program for determining when aphids switch from one form to another. In other words, the dependence of the adaptive values of roundness or flatness on the frequency of these two types has tuned the genetic “switch” to be flipped in response to changing frequencies.)
Finally, one can contemplate the difference in evolutionary strategies of the two forms, one mutualistic and the other parasitic. But here I’ll simply reproduce what the authors say:
The dual strategy developed by the aphid P. cimiciformis outlines a complex evolutionary scenario. On the one hand, the round morph and the ants, engaged in a trophobiotic relationship, should be subjected to the conflicts of interest typical of mutualism, with selection driving each partner to maximize its benefit by giving the least of its own energy and resources. On the other hand, the flat morph and the ants can be expected to be engaged in an arms race, with selection favoring improved deceiving abilities in the aphid and increasingly finer discrimination abilities to detect noncolony members in the ants.
By the way, if you go to the paper’s website, you can see three bonus movies of ant/aphid behavior and interactions that don’t appear in the paper.
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Salazar, A. et al. 2015. Aggressive mimicry coexists with mutualism in an aphid. Proceedings of the National Academy of Sciences 112 1101-1106; published ahead of print January 12, 2015, doi:10.1073/pnas.1414061112
Fascinating — many thanks.
The complicated relationships between benefit and aggression here seem almost Machiavallian. Evolution is a simple idea at its core, but it isn’t simple.Yikes.
Very interesting. Evolution sure generates weird relationships.
I very much enjoy the mimicry posts. I have often wondered at what level mimicry, or possibly, the idea or knowledge (anticipation) of predators plays a role in non-living things.
Does mimicry require life? Are there inanimate objects that work on a principle of mimicry, i.e., trying to be like something else because it might be energetically or thermodynamically more favorable? I am not sure.
Clearly, we can program bots to possess qualities that would appear like avoiding predation. We can design drones that would recognize a situation that it’s better to change appearance into something innocuous in order to ocmplete mission. Mimicry can be designed.
Mimicry is in art as well. Art looks at reality and recapitulates that reality. If art fails to emulate, it usually fails. Great art transcends, even reproduces: the zeitgeist of today’s ministrals and poets and painters inform, directly, the next generation. If the art does not, then that art usually perishes.
Such an interestingly weird question. Cheap knock-off products mimic name-brand products. Alternative medicine ‘doctors’ mimic real doctors. Of course they are alive…
Mimicry evolves via natural selection, which in turn requires reproduction with inheritance and differential survival to operate (not to mention a lot of time). Sounds like a definition of life.
The examples you cite are of artificial selection. It seems reasonable to think of mimicry as a foundation for invention, but that still involves an animate inventor.
We can be a little loose here b/c it is fun, and not too wacky.
Product designs evolve, with variation (innovation, etc.) and selection (in units sold).
Furniture evolves. The curved footed legs of some chairs and tables are descended from ancient thrones where furniture was crafted to explicitly look like lion legs. The qwertyuiop arrangement of buttons across a smart phone is descended from the arrangement of keys in manual typewriters. In button down shirts men’s shirt buttons are sewn on the right panel, but women’s shirt buttons are sewn on the left panel. There is a historical reason for that.
Really interesting. Lots of angles to pursue with this system, clearly.
One is about nutrition in aphids and their endosymbionts. Aphids feeding on plant sap do not get enough amino acids, and so they use endosymbiotic bacteria in their cells which make the amino acids for them. A picture of bacteria in aphid cells is found
here. The roundish, speckly things crowding together are bacteria inside a cell.
But the aphids feeding on ant larvae may not need the bacteria, so what is going on with their endosymbionts? They would be passed on thru the eggs, but are their numbers reduced b/c they are not needed? Maybe the endosymbionts have something to do with the morphology and smell and behavior of the aphids.
Interesting suggestion!
It is possible to imagine that the endosymbiotic bacteria would be not so well adapted to the secondary host and in some clonal lines would become too rare or too feeble to be useful, what would trigger the white-flat phenotype, feeding on a proteinic diet. The situation would be re-established in the next sexual generation on the primary host. Just a wild guess, of course.
Maybe a frequency dependent selection based evolutionary arms race between the bacteria and their aphid hosts, for what I do not know. Plans and schemes…😈
How are endosymbionts partitioned into the eggs? Randomly/equally? Is there variation on this? Also, the GCgraphs show qualitative differences in a few compounds (8/9, 20/21, et) but substantial quantitative differences as well for a number of peaks – would like to know what some of these are, pathways (can’t access the paper) – a shift in expression of one or two single genes, possibly in response to endosymbionts (or lack) might possibly produce an array of biochemical variants.
Realy really interesting!
I like the “frequency-dependent selection” idea as it applies to so much in the natural world including human behaviour(s). It is why we sometimes find it advantageous to cheat or sometimes cooperate. It also means that rich and poor people have an ‘advantage’ (maximize descendants) in having male offspring, while those in the middle ‘benefit’ from having daughters.
I should clarify – cheaters will always remain at some level in a population as that behaviuor can have an advantage even if there is no ‘cheating gene’. If everyone was cheating it would lose value as a behaviour.
Perhaps the comparison is not as good as that is behaviour rather than genes (but then we don’t know exactly the cause in this aphid) – maybe eye colour – light eyes might have an advantage in lower light where darker eyes would be a disadvantage etc…
I remember seeing the mutualistic behavior in a nature film in grade school. It made me really mad that the bad guy aphids “paid” ants, Mafia-style, to attack ladybugs – it’s interesting to learn a little more about the mechanism behind it.
Thanks so much for letting me know the aphids also prey on the ants. It feels like justice.
And I wonder how the two-form “strategy” might be mutually reinforcing: might the ants’ protection racket somehow reward the round form in a way that keeps the flat form from dominating, and might attacking the brood make the ants more dependent on (or eager to reward, for survival) the round aphid somehow? That kind of mechanism would be consistent with the authors’ last paragraph, as well as with several plotlines of The Sopranos.
On the surface the two-form strategy sounds crazy, but I look forward to hearing the theory that pulls it all together.
The whole, “trick you into smuggling me into your nursery so I can eat your babies” thing does seem like something Phil Leotardo would do.
LOL Phil Leotardo! “Say ‘bye-bye’ to Grandpa!”
I always like this sort of article, as it illustrates how *deep* we’ve really gotten in our understanding of things and yet also how far we have to go. In other words, what science is really like! (The expanding frontier.)
I enjoyed getting to know these amazing creatures!
Admittedly most of the sum total of my knowledge of aphids comes from the article posted directly above, but the, for lack of a better term, Trojan Horse hunting strategy seems very sophisticated for such a creature.
This stuff is so cool. Even if it takes me several passes to get a grip on the material and some of it is just obtuse to me due to my lack of education in biology, I love these types of posts.
The chemical mimicry alone is fascinating, but the life cycle, and the many forms that these aphids can take is mind blowing. I have to get back to routine errands and paperwork, but I’ll be in awe for the rest of the day thinking about this. Great post!!!
Tremendously interesting post, thanks. Like others here, I had heard of the aphids who are kept by ants for their honeydew, & I was aware that there are predators who attack the larvae, but I was not aware that one critter does both. To me, the chemical mimicry is less interesting than the dual morphs & their widely differing strategies. Is it safe to guess that the round green version might have been free-living originally, then joined up with ants in a mutually beneficial arrangement, only after which the flat white form would develop?
Great article! I really enjoyed it, enjoy though I think some of it went over my head. This might seem like a silly question, but:
What do the aphids do after they have been carried to the brood chamber and fed? Do they make their way back out of brood chamber and the hive? Are they able to do this, considering that they were carried to the chamber in the first place? With their hydrocarbon profile aren’t they at risk of being carried back to the brood chamber perpetually by ants they happen across on their way out? Is there something simple that I’m missing here?
“the round ones have an advantage because the ants’ brood will be diminished so severely that the colony may go extinct, endangering the survival of all aphids associated with the colony”
Is this not group selection or perilously close to it? The next sentence sounds like E.O Wilson might have written it.
(“This becomes more probable when many aphids are clones, because selection on one is selection to precisely the same degree on clone-mates.”)
Yes, I wondered that question as well. I don’t know how these aphids reproduce, but if it is not like bees, wasps, and ants – with a single queen donating her genes to all members of a colony, then it does sound rather like they are adapting as a single entity – a group. Does Ceiling Cat have an opinion?
The caption of Fig. 1 tells us how these aphids reproduce, and during the phase in question, it’s by parthenogenesis. So it’s not a question of parasitic morphs competing with mutualistic morphs. Rather, it’s genome A competing with genome B, where A and B produce different ratios of parasitic to mutualistic morphs.
Clones that over-parasitize will decimate their host ant populations, to the detriment of their own success. Clones that under-parasitize will fail to exploit feeding opportunities. Clones that strike the right balance will flourish along with their ants.
No group selection needed; just genes competing against genes for their own advantage — albeit in many bodies per genome rather than just one.
but that exactly describes group selection, groups with a certain deleterious trait (under-parasitization)will outcompete other groups with another seemingly beneficial trait (aggressive parasitization). Granted I agree with the good professor’s argument, but I think this is an instance where group selection is possible; when one’s group is subject to extinction, traits can be selected for at a higher level than the gene or individual. I think group selection has difficulty explaining selective pressures without evoking extinction as a mechanism.
Group selection, as I understand it, is meant to reward groups whose members act against their own selfish reproductive interests for the good of the group.
But in cases such as these aphids, where the group comprises a clone of genetically identical individuals, the reproductive interests of the group are identical to those of the individual: to pass on (copies of) their shared genome. So there’s nothing for group selection to select for that regular selfish-gene selection doesn’t already accomplish.
Note that you and I are also groups of genetically identical units (cells) whose reproductive interests are aligned with those of the group. Is it therefore “group selection” when one of us outbreeds the other? The only difference between this case and the aphid case is whether the genetically identical parts form a single connected body or multiple bodies.
Thanks for filling in the blanks.
Wow, what a fascinating world we live in!
Jerry, I have nothing concrete to add, especially in view of the many informed comments above; but given your doubts a few months ago as to whether your detailed science posts justified the work it took to write them, can I just say Yes, every time! I find them endlessly fascinating and am so grateful to you for keeping my education going.
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What he said.
Same here.
Fourth the motion.
Reminds me of the reef cleaning stations, and the fish that mimic the cleaners to bite the cleanees.
Thanks for the superb post.
Based on this:
“On the other hand, the flat morph and the ants can be expected to be engaged in an arms race, with selection favoring improved deceiving abilities in the aphid and increasingly finer discrimination abilities to detect noncolony members in the ants.”
So if the ants were to get the upper hand and detect the flat aphids, would they become tolerant of the aphid’s hydrocarbon profile and ignore them (not bring them to their brood chamber) or would they become aggressive and actively harm or kill them?
I wonder how long it took the scientists to figure all this out. Kudos!
My favorite post in weeks! So many interesting species, behaviors and relationships in a bug’s world. Praise Ceiling Cat for forms big and small!
Don’t have time to read this at work right now, but I will make time to read it tonight.
b&
This is awesome. A Dr. Jekyll and Mr. Hide Aphid. The thin line between mutualism and parasitism -and the latter inevitably causing arms race. And the fact that we as visual mammals (itself quite outlying) tend to forget there is other mimicry than visual mimicry. It has it all.
Wonder if this within-species Jekyll/Hide scenario is more common than just in this particular aphid. Well, I guess we all suspect so, this discovery may have touched something. It may even be pervasive throughout nature.
Thank you for this thought- and speculation-provoking post.
I don’t have much (anything) to add to this discussion, but I wanted to take the time to comment as you’ve complained in the past how much time and effort it takes to compose compared to the religion pieces. Stuff like this is why I started reading WEIT in the first place. Thank you.
Very cool, and so complicated it could not have evolved. Ergo God. And if God micromanages such little things, he surely gets involved in other minutiae like football games, too. Now Merkins can sleep better.
Holy fucking shit, that was mind-bending and -expanding!
So…the question that’s bugging me…would it not be to the advantage of the ants to retaliate against just the species of aphids that makes the round vampires even when they’re in their friendly flat form?
I’ve no clue how something like that could arise…but it would seem that, if it did, it could provide a significant benefit to the ants.
Is there anything in there about whether or not the ants favor flat Jekyll-and-Hyde aphids over “regular” ones?
b&
Absolutely fascinating. And so great to be thinking about biochem again, after being away from it so long. This goes into my files, so I can revisit from time to time.
Interesting read, thanks!
Commenting for the first time to say thanks for this fascinating article! It always boggles my mind to learn about the incredibly complex and finely tuned systems evolution can produce.
Also, I noticed a minor typo: in the sentence “But how the flat form evolved from the white form, …” it looks like the word “white” should be replaced with “round”.
Reblogged this on Mark Solock Blog.