by Matthew Cobb
One of the big problems that worried Darwin in his theory of evolution by natural selection was what he called ‘the example of neuter insects’ – social insects such as ants, wasps and bees—groups in which most of the members of a colony are female, and yet do not reproduce and are sterile. As Darwin wrote in On the Origin of Species:
Darwin’s answer was that selection operated at the level of ‘the family’ – sterile workers shared characters with those individuals who were reproducing, and thus those characters could be ‘seen’ by natural selection.
We now interpret worker sterility in terms of genes shared by highly related groups of insects, which in the case of Hymenoptera (bees, wasps and ants) show a bizarre form of sex determination called haplodiploidy, whereby males are haploid, produced from unfertilised eggs, while females are diploid, produced by mating.
This means that if a queen has mated with only a single male, her offspring (the workers) are more closely related to each other (sharing 75% of their gene copies) than they would be to their own offspring (50%). In other words, it is in the genetic interest of the workers to be sterile and rear their sisters rather than mate themselves – they will pass on more copies of their genes to the next generation this way!
Life is (of course) more complicated than this – many queens mate with more than one male, so those ideal relatedness levels aren’t always seen. Furthermore, while haplodiploidy encourages the evolution of sociality, it isn’t necessary. Many Hymenoptera are not social, despite being haplodiploid, while some of the most successful social insects – termites – have XY sex determination like you and me.
However, for the last few decades the basic view of those studying sociality has been that it’s in the workers’ genetic interest to be sterile – they are passing more of their genes on to the next generation this way. They haven’t been ‘sterilised’ by the queen, they are ‘choosing’ to be sterile (or at least, choosing not to mated, for in some species workers can produce males from unfertilised eggs).
This would mean that for a worker to turn off her ovaries, she would need two bits of information – she is surrounded by closely-related individuals (that is, there is a colony-specific signal) and that there is a reproductive individual present who is churning out eggs (that is, there is a fertility signal provided by the queen or reproductive).
There were two reasons why we came to this view. Firstly, in 1993 there was an excellent article by Laurent Keller and Peter Nonacs which looked at what we would expect if the queen was controlling the workers, or if she was merely signalling her fertility and thereby enabling the workers to ‘decide’ to turn their ovaries off. Keller & Nonacs pointed out that if the workers were being forced into sterility, then there would be an ‘arms race’ and in some groups we would expect to see that workers had started mating. So you might expect, for example, to see some species of solitary ants. There is no such evidence, so on the basis of a tight argument, most people accepted that there was no evidence for queen ‘control’. That doesn’t mean to say it doesn’t exist, merely that there is no evidence of this.
The second reason is that there was a mass of evidence showing that chemical signals are involved in affecting the growth of worker ovaries. If you removed the reproductive individual from the colony, in some species worker ovaries would soon start to grow. Furthermore, the chemical signature of the reproductive is correlated with her ovarian function – these ‘queen pheromones’ are in fact a chemical signal indicating her fertility. Further, similar effects were seen in solitary insects, like flies, providing an insight into how the sensory systems of social insects could have evolved, on the basis of the pre-existing sensory systems of solitary insects.
As Michel Chapuisat puts it:
The hypothesis that queen pheromones evolved from a preexisting communication system in solitary ancestors has interesting implications for the evolution of eusociality. In the early stage of sociality, daughters may respond to maternal fertility signals by helping the mother if she is highly fertile, and reproducing if she is not. By allowing this conditional response, a preexisting pheromonal communication of fertility may have facilitated the transition to eusociality.
In the latest issue of Science there is a stunning proof of this suggestion (Chapuisat’s article is commenting on this), but frustratingly it is partly framed – and is certainly being reported – in the wrong way.
To summarise an awful lot of very impressive work, the scientists looked at three very distantly related species – a wasp, a bumblebee and an ant, in each of which sociality evolved independently (in other words, their most recent common ancestor was a solitary insect).
They looked at the chemicals on the cuticles of the various castes within these species (queens, workers, males), and identified a set of compounds that appeared to be common to the queens in these species. They then removed the queen from colonies of these insects, and introduced synthetic versions of the compounds, and observed what happened to the workers’ ovaries. If the ovaries remained regressed, then this would indicate that the compound was perceived as indicating the presence of a queen.
Amazingly, they found that some of these compounds were indeed common to these three groups (note the effect is clearer in the wasp and the ant – which are more closely related – than it is in the bee):
The legend says: “The results demonstrate that long-chain cuticular hydrocarbons act as a conserved class of sterility-inducing queen pheromones in three independently evolved social insect lineages, represented by the wasp V. vulgaris (A), the bumblebee B. terrestris (B), and the ant C. iberica (C). Treatment of queenless worker groups with the linear alkanes n-C27 and n-C29 and the methyl alkane 3-MeC29caused a two- to sevenfold reduction in the odds of workers having fully developed ovaries in the common wasp and the Iberian ant (bar charts, red bars) relative to a pentane-treated control (left, stacked bar charts)”
So this suggests that there may be common chemical signals relating to ovarian function that are used in all these species. The authors then looked at a large number of other studies and plotted the putative fertility signals onto a phylogenetic tree, with fascinating results:
The legend says: “Fig. 2 The evolutionary history of queen and fertility signals across major clades of social hymenopteran insects. Each alternately shaded clade indicates an independent origin of eusociality. The pie charts show the likelihoods of different compound classes being used as queen or fertility signals (…). Saturated hydrocarbons (linear and methyl-branched alkanes) receive very high support for being used as conserved queen or fertility signals across several independent origins of eusociality.”
The authors conclude with this great summary of a marvellous piece of work:
“our ancestral state reconstruction shows that saturated hydrocarbons were most likely used as fertility cues in the common solitary ancestor of all ants, bees, and wasps, which lived ~145 million years ago”.
Note that they aren’t suggesting that exactly the same molecules are used today – “saturated hydrocarbons” is a pretty broad class of substances, and insect physiology keeps on popping up with the same molecules (they’re all related to fatty acid biosynthesis), so this is an entirely legitimate suggestion.
So what’s my beef? The data are fantastic and change the way we think about the evolution of queen signals, suggesting the same signals may exist in different lineages. The problem comes with the way the findings are being presented. Here are two screenshots from the Science magazine website. See if you can spot the problem.
Both these presentations – especially the second one – suggest that the authors have proved that queens control their ‘underlings’. My guess is that this view will be repeated in the media over the next few days. In fact, the study does nothing of the sort – it doesn’t show how these chemicals exert their effect. If anything, as the authors argue, and emphasised by Chapuisat, it supports the view that these are fertility signals, not methods of ‘control’ used by the queens ‘to prevent worker reproduction’. The idea of ‘underlings’ being ‘controlled’ might seem sexy to some; to anyone who knows, it’s just plain wrong.
So where does this view come from? It’s not simply sub-editors at Science who don’t ‘get’ what is, I accept, quite a subtle point. I fear the authors have inadvertently contributed to the confusion.
The title of the paper is ‘Conserved class of queen pheromones stops social insect workers from reproducing’. To which I would answer, ‘well yes and no’. The ‘stops’ is very affirmative and suggests strongly this is a manipulation of the workers’ fertility by the queen. Elsewhere in the paper, they suggest ‘pheromones emitted by the queen are thought to play a key role in suppressing worker reproduction’, ‘we searched for sterility-inducing queen pheromones’, ‘the more volatile queen pheromone blend not only stops workers from reproducing’.
These minor terms create the impression that these compounds act against the interests of the workers. This might be the opinion of some of the authors, or they might have felt that this was a sexier way of presenting the findings, or it might just be sloppy writing. Whatever the case, it’s unfortunate as it lessens the impact of a fantastic piece of work.
Why do I care? Well apart from being punctilious/cranky, I have 150 final year students sitting a Chemical Communication in Animals exam on Monday, and I don’t want them to go off writing about this new study showing queen control!
A final intriguing point. About 15 years ago, Jean-François Ferveur and myself, together with two of his students, suggested that closely-related Drosophila species (the flies studied by Jerry) might use common sex pheromones, which are related to ovarian activity. Among the compounds we suggested could be involved were saturated hydrocarbons such as 2-methyl hexacosane, 7-heptacosene and n-heptacosane – chemicals with structures similar to those identified as common fertility signals in social insects by this study. The deep history of chemical communication in insects might go even further than anyone had suspected.
[UPDATE: I told you so. Here’s New Scientist’s coverage of the article. *Sigh*. “Minions”. They should know better, but maybe it’s me who should not expect so much from them… h/t @dunbarrover]
References (mostly $$$ I’m afraid, but the link will get you to the abstract):
Chapuisat (2014) Smells Like Queen Since the Cretaceous. Science 343:254-255
Sorry if I’m being dense, but I’m having a tough time decoding that first figure. What are the “odds ratios” they’re talking about? What do the red and blue bars above and below the line measure, and how do they relate to the stacked control bars at the left?
Sorry, it is confusing. Up indicates a component was more likely, down indicates a component was less likely to have an effect either allowing the ovaries to develop (red) or regressing them (blue). So for example in the bumble bee nC25 increases the probability do regressed ovaries, but removing it doesn’t tend to lead to developed ovaries. I don’t know what the left hand column means and don’t have the paper to hand. Can anyone help? If not I’ll answer tomorrow.
I now notice that the graphs show a weird illusion – the horizontal line at 1 does not look horizontal to me – it slopes down to the right. It doesn’t (I’ve checked!), but it looks odd…
I thought I was dense too because I couldn’t understand it either.
Excellent summary and write-up, and I especially agree with the oddly queen-centric framing of this issue in some of the coverage.
One minor quibble, though. Recent research by Ward et al in Current Biology ( http://www.cell.com/current-biology/abstract/S0960-9822(13)01056-7 )suggests that the ant & bee are actually the closest pair, rather than the ant & wasp.
Thanks Alex. You are of course dead right about Phil Ward’s paper. Old habits die hard, especially when the new result is so surprising!
I’m curious about what the story is for termites.
I would like to see that explained too! The theory of how eusocial societies evolved in insects tends to focus on the weird ‘haplodiploidy’ genetics of wasps, bees, and ants, but I have not seen an explanation for termites where both the reproductive caste and the worker castes are diploid. I guess it boils down to ‘kin selection’, where workers defer reproduction to their kin. Their queens and kings have huge reproductive success, more than the workers would if the workers reproduced. Not sure if that is right, though.
Well, there’s no genetic disadvantage to eusociality even in regular diploid species. Having full siblings is just as good as having offspring of your own. So it’s a question, as you say, of whether having specialized castes for reproduction, nurturing, etch, rather than everybody trying to do it all, makes for greater per-capita reproductive efficiency.
Apparently for termites and mole rats it does.
“Etc.”, not “etch”.
The mole rat connection was exactly the parallel example I was looking for. Thanks.
Koos Boomsma suggests the “monogamy hypothesis”, where life-time monogamy without the potential to re-mate is the crucial step in the evolution of sociality. Read his 2007 article “Kin selection versus natural selection: why the two ends do not meet” (http://www.sciencedirect.com/science/article/pii/S0960982207015709)
This is something that’s bugged me periodically, though it’s not very close to anything I do, so I’ve not put much effort/thought into it. But, I’m still not totally convinced — in fact, I’m a bit more confused after reading this. I obviously need to read it again and think more carefully.
Why shouldn’t the issue be the fitness of the queen/reproductive? A queen that produces lots of sterile workers that help raise the next generation of queens could have higher fitness, if that results in more reproductives in the next generation than with the alternate strategy of just producing lots of queens right off. Couldn’t this be viewed as analogous to the germ/somatic line division in mammal bodies? What does it mean to talk about the fitness of workers? How is that different from talking about the fitness of muscle fibers? I know that the haploid male issue is going to play into that.
Plus, how does the existence of a few ant species where workers are potentially reproductive affect this? For example:
“One such species is Jerdon’s Jumping Ant (Harpegnathos saltator). They usually live in colonies smaller than 100 individuals and workers may reproduce, so the colony can survive after the queen’s death.”
It sounds as if, assuming that account is accurate, this could be a case where the presence of the queen, and her highly conserved pheromones, might suppress reproduction in workers.
Score me as confused for the moment.
Workers aren’t like muscle fibers in that they have their own genomes that are distinct from the queen’s. So the worker’s genetic interest is not precisely aligned with the queen’s, and workers pursue their own interests, not the queen’s.
I believe this has been demonstrated with regard to sex ratios. If I’m remembering the details right, it’s in the queen’s interest to produce a 50:50 sex ratio of offspring — and she does. But because of haplodiploidy, it’s in the workers’ interest to enforce a 3:1 female:male ratio in the nursery — and they do. The queen lays more male eggs than the workers care to nurture, and they discard the excess.
I think Dawkins covers this in The Selfish Gene.
Also well described by Ed Wilson (of course).
Do you remember where? In Ants, I expect.
I have 6 of his books before me (7 if you count Island Biogeography) and can’t find any discussion of this.
The Selfish Gene Chapter 10, You scratch my back, I’ll ride on yours deals with this. In particular, pp198 to 202 in the thirtieth anniversary edition.
The abstract of the Trivers and Hare article this is based on is here: http://www.sciencemag.org/content/191/4224/249.abstract
I remember it from reading Sociobiology many decades ago. I would be amazed if it wasn’t richly described in The Ants. (Although I have not read that book.)
I remain puzzled. Sorry!
“Workers aren’t like muscle fibers in that they have their own genomes that are distinct from the queen’s.”
But they’re not reproductive, so natural selection can’t see that difference can it? Besides, somatic tissues of mammals have their own genomes too that are somewhat distinct from the germ line — liver cells are polyploid, any tissue can have somatic mutations, etc. Small difference, but irrelevant? Does my liver have different interests from the rest of me?
“So the worker’s genetic interest is not precisely aligned with the queen’s, and workers pursue their own interests, not the queen’s.”
But the workers “interests” seem tightly tied to those of the queen, even if not identical, since they cannot reproduce and she can. The only way any of their genes are going to get into the next generation is through the queen. Right? Except that there are genes from the male parent in the sterile workers, and those are not present in the queen. How can those male derived genes get into the next generation except through the sisters of sterile workers? That is, through new queens produced by the existing queen. It seems the interests of the genes of the sterile workers is served by the production of queens in the next generation — nothing else seems to move the whole set of their genes along. Males, brothers of the sterile workers, have only a set of genes from the existing queen, since they’re haploid.
“I believe this has been demonstrated with regard to sex ratios.”
I’m going to try to find out more about that — the business of manipulation of ratios by workers. This may be the critical thing I don’t understand.
“I think Dawkins covers this in The Selfish Gene.”
Can’t find my copy at the moment. Haven’t read it in at least 10 years and may have to acquire another. He doesn’t seem to talk about this in “Climbing”, “Watchmaker”, “Unweaving”, “Show” or “Ancestors” which are the things I can immediately put my hands on.
Dawkins does mention slave-making ants — are those a problem here? Slave workers share “nothing”(except more general ant genes) with the brood, but they work for their benefit or even may tend them directly, I think. Pheromone control of alien workers by the queen?
I’m still not clear on why anyone is sure what the answer is. The referenced Science paper seems to say it’s “queen control” so the alternative hypothesis is not universal, even if dominant.
Sure it can, through kin selection. If a gene residing in a sterile worker causes that worker to behave in such a way as to benefit fertile siblings carrying the same gene, that’s natural selection operating on the worker’s genes, not the queen’s.
Tumors arguably have different interests from the rest of you. (But I’m not going to argue that point very strenuously.)
Sure. But by the same token, the only way the queen gets her genes into the next generation is through the nursery. The queen controls what sort of eggs get laid, but the workers control which of them survive, what they get fed, and whether they grow up fertile or sterile. So that gives natural selection a means by which to distinguish the queen’s success at propagating her genes from the worker’s success at propagating (copies of) theirs.
Good, but the critical thing, in my opinion, is not the sex ratio (that’s just an easy-to-measure test case) but the fact that the workers control a portion of the reproductive pipeline, and therefore have an opportunity to promote their own genetic interests (as distinct from the queen’s) by filtering what gets through to maturity.
Sorry for being dense. Thanks for the patience of all who have commented during my struggle to understand this. I’ve read all your comments and found my copy of Selfish Gene and read the relevant section — I finally see the argument properly, I think. I’ll comment at greater length this evening, but of course by then the topic will be buried under others.
I do have to say that the genetics of hymenoptera are very odd, but educational!
I think you will feel less confused if you put aside the idea of “dead end bodies” for a while, and consider what is happening to gene frequencies in these populations, and the degree of relatedness between the various castes involved.
The queens have a fifty percent relationship to both their daughters, and their sons.
The sons have 100% of their genes in common with their mother, but have only half her genes.
The workers have on average only a 25% genetic similarity with their brothers.
The workers have on average a 75% genetic similarity with their sisters including new queens.
The optimum outcome for the existing queen is a 50:50 split in resources between male offspring and daughter queens. This is reflected in the gender ratio of the eggs she produces.
The optimum outcome for the workers occurs when 75% of reproductive resources go to producing new queens, and 25% to males. This is the ratio of resource allocation that is typically measured in monogynous ants. In these cases the workers are winning. Their interests are most closely represented by the daughter queens, not their mother. They don’t need to directly reproduce, they just need to control the reproductive outcome.
Slave ants are raised from the larval stage in the slaving colony. They need no extra pheromonal control. They act as if it is their native colony.
Slaver queens have relatively little genetic information in common with the slaves. The slaves have no opportunity to evolve mechanisms that will see through mechanisms that hide the gender of the eggs that slaver queens produce. In these cases we tend to see a 50:50 split in reproductive resources between males and new queens. The slaver queens are winning.
There is nothing in the data and discussion that Matthew Cobb presents from the Science article that suggests “queen control”, though there is the pair of sensationalist screenshots, a misleading title, and some editorialising. What is actually presented is a mechanism of chemical communication that could equally be part of either scenario.
Sorry this is so long, but there is a lot to cover, and it only makes sense in terms of populations and degrees of relatedness.
I think some of your questions can be extended to, “why do human females persist beyond menopause”. They have no reproductive value. Clearly there is some other value. I’ve heard speculation that it is because they help raise children. It’s perplexing how they would be selected this way but clearly something clicked.
Consider an analogy, involving a CEO and a board of directors for a public corporation.
If the stock price is rising, and profits are increasing, the board is not likely to appoint a new CEO. Does this mean the current CEO is suppressing that appointment? Or is the board suppressing itself, using the performance figures as signals?
It might seem like a matter of semantics, but only if you ignore that most important question, which sounds so much more impressive in Latin: cui bono?
In order for a relationship to be one of suppression, rather than signalling, the putative suppressor must benefit more than the suppressed. That means the genes in the queen must do better than the genes in the workers. If that were the case, you’d expect some insurrection, with bees reverting from eusociality to single living. The apparent absence of this lends support to the notion that the answer to the question cui bono? is the worker bees, who suppress their own reproductive capacity when in the presence of the queen’s fertility signals.
As for your earlier question regarding greater fitness by having more reproductive offspring, that’s basically begging the question. The whole premise of eusociality is that reproductive success is higher with hive living and limited fertility, which is why it evolved in the first place. Exactly how is what everyone studying them aims to find out.
The genes of the queen are in the workers and the workers can’t reproduce — they are dead ends. The issue is what gets the most genes into the next generation and why? There must be an advantage to sociality, it must move more genes down the line under some circumstances, but how does that system arise? I’m not seeing a convincing answer, but admit I don’t know much about it. But, the fact that the new Science paper argues for a different interpretation suggests to me that more work is needed (as usual).
“Exactly how is what everyone studying them aims to find out.”
I agree. It doesn’t seem everyone agrees on the answer, so folks are still trying to find one. I wonder if there even is a single answer — maybe sociality has arisen more than one way in hymenopterans. It clearly arose a different way in termites.
There is an apiary at the Abbey of St. Thomas where Mendel worked. He intended to study the genetics of bees, but, fortunately, moved into administration. I think he would have been utterly confused by haplodiploid inheritance.
Maybe the authors that referenced the results are bit Marxist and saw the workers as proletariats. You can’t help but start to think that way with words like “queen” and “worker”.
Reblogged this on Mark Solock Blog.
Thanks from a long time beekeeper. And yes we do read the techie articles it is just sometimes harder to add our two cents.
Beekeeping is a very critical industry, and a great hobby. I am always amazed at the many little tricks of the trade for tending the hives, keeping them from swarming, and so on.
Yes, it seems to be pretty tricky. I can barely deal with my fish tank!
Commenting only so that Jerry will know I read it and not be discouraged that no one reads the science posts. It’s fascinating, but I have nothing interesting or humorous to add.
I’m now quite curious to know if similar sorts of chemical signaling happen in eusocial mole rats. And especially curious to know, if so, if there’re any similarities in the actual chemicals themselves.
b&
There is perhaps a bit of the determinism versus free will question here. Is there really a difference between a queen suppressing the reproductive activity of workers, versus workers suppressing it themselves in response to a signal from the queen? The queen produces the substance, and reproductive activity in the workers is suppressed, and it is just some biochemistry taking place. If that works out better than not having it so, it will be positively selected.
Better for whom? Again, the interests of the queen and of the workers are not exactly parallel. So yes, there really is a measurable difference between workers pursuing their own interests and being coerced into serving the queen’s.
“The queen produces the substance, and reproductive activity in the workers is suppressed, and it is just some biochemistry taking place. If that works out better than not having it so, it will be positively selected.”
That’s what I’m thinking. The thin (semantic?) difference between control and signaling also seems an important point for consideration to me.
Whether or not the next generation of ants is closely related to the workers is irrelevant.
The workers have no say in whether they can breed or not. When a fish lays thousands of eggs and only one or two survive nobody says that the ones that are eaten are close relatives of the survivors it doesn’t matter that the vast majotity of ants are sexless and will not breed the strategy which allows the organism to continue works and it does not even matter it the new generation has a difference so long as they continue to thrive.
This all seems to be a very significant finding concerning the evolution of the social insects and of the nature of insect society (though for me somewhat difficult to follow) But is it the ULTIMATE explanation of worker sterility in these species (particularly termites)? The chemical processes at work seem to me a proximate cause of this sterility, not ultimate. Has this chemical inhibitor come in play only to reinforce a fundamentally useful survival strategy in these species? (If the strategy itself were not strategically effective some mutant strategy avoiding the chemical inhibitor and allowing individual reproduction would take over) Perhaps E. O. Wilson is right, and we must turn to group selection for an explanation.
What gets me is that such a simple set of compounds are being used – and, it would seem, being highly conserved – as signalling compounds. Really I would have expected the structural diagrams to resemble the results of going spider hunting with a cricket bat. Probably with a couple of dozen heterocyclic centres in there, and a chirality situation that would daunt constitutional lawyers acting for the NSA. (Or NRA ; same difference?)
Mostly straight chain alkanes. Was it one with a methyl branch at position 3? That is just so … so … well, if I can understand the structures from their formulas, then it’s shockingly simple compared to “real” organic chemistry. Something about using such simple compounds has a real advantage there. I don’t know what it is, but that stinks of really intense selection pressures.
OK : I’m a rock sniffer, not an ant/ bee/ wasp/ termite sniffer. But that is just weird. I have to deal with more complex structures which have been torn down and re-built by heat, time and water ; that chemistry doesn’t look “organic”. It’s not complex enough.
Hey there,
I’ve just seen this piece now! Thanks for writing it, glad you enjoyed our paper. It’s great that you stress the distinction between a pheromone “controlling” one’s behaviour, and it “controlling” one’s evolutionary interests. For example, just because workers exposed to queen pheromones become more sterile than control workers, doesn’t mean the pheromone is manipulating workers to their detriment (there is now a whole review aimed at sorting out this misconception by Peso et al http://www.ncbi.nlm.nih.gov/pubmed/24925630).
Many people have been confused about the meaning of “control” when it comes to pheromones; my theory is that people think of chemical communication as more drug-like than, say, visual or auditory communication, so they assume the receiver has less power to respond adaptively to the signal (obviously, one needs to consider fitness to say much about fitness consequences of pheromones). One example concerns a series of discoveries that the honey bee queen pheromone affects gene expression and dopamine levels in workers’ brains; some folks called this a clear case of brainwashing/manipulation by the queen, though actually one would need additional evidence to make that claim, since mutually beneficial signals would also affect worker phenotypes.
I always try to make this very clear in my writing, so it’s a shame you thought we were being sloppy here! To be fair though it’s a hard job. Take the phrases you didn’t like: “sterility-inducing queen pheromones” and “queen pheromone … stops workers from reproducing”. I can’t think of how to improve over those; the pheromone DOES induce sterility, and it DOES stop reproduction. These are just blank phenomenological descriptions of what happens, IMO, although some readers infer adaptive meanings from words like “stop”, “induce”, and “inhibit” (if you think of a word meaning “to stop something from happening” that doesn’t incur this problem, it’s be genuinely helpful).
If you aren’t bored of this topic yet, you might enjoy my recent paper which is a model inspired by these data (specifically, the result that chemicals that encode information on a female’s fertility could pre-date eusociality). I argue that knowing how fertile their mom was could have allowed proto-workers to employ conditional helping strategies, and thereby helped species across the difficult boundary into eusociality by way of a “warm up” phase with facultative sociality. Here it is: https://docs.google.com/viewer?a=v&pid=sites&srcid=ZGVmYXVsdGRvbWFpbnxsdWtlaG9sbWFufGd4OjE1YmNjYWYyMjk0Nzc3ZGQ