Fertility signals in ants, bees and wasps have deep common origins

January 20, 2014 • 2:18 pm

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

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.

Bee
bee2

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]

NS

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 

Keller and Nonacs, (1993) The role of queen pheromones in social insects: queen control or queen signal? Animal Behaviour  45:787–794

Van Oystaeyen et al. (2014) Conserved Class of Queen Pheromones Stops Social Insect Workers from Reproducing. Science 343:287-290 

Fabrice Savarit et al (1999) Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation inDrosophila. PNAS 96:9015–9020

Readers’ wildlife photographs (i.e., moar birds)

January 20, 2014 • 1:25 pm

For some reason, the wildlife photos that readers sent me are about 90% pictures of birds. Where are the mammals, the insects, the plants? Well, I can’t complain because I do love a good photo of our feathered friends.

Reader Bruce Lyons sent in some nice bird photos, and a description of where and how he took them:

I live at the base of campus at the University of California in Santa Cruz. The photographs were all taken from within my house, looking out an open window into the canopy of a hawthorn tree that brings in the birds.  We call it Bird TV—just sit, watch and the activity come to us. We get lots of frugivores coming in to eat the berries—robins, waxwings, hermit thrushes, among others.  Interestingly, waxwings are far more likely to hit the windows than any other species and we suspect it has to do with the way they leave the tree as a flock, perhaps as an anti-predation mechanism. Raptors learn that fruit trees are bird magnets and we occasionally see Cooper’s and sharp-shinned hawks going for birds in the hawthorn tree.

A hummingbird feeder near the window also brings in Anna’s Hummingbirds (you recently posted a video of a male courtship flight) and I will also include a couple of photos to show what a male Anna’s hummingbird looks like close up (short answer is spectacular). The hummingbird photos were taken on a rainy day so the bird was covered with tiny water drops and his gorget colors just glowed.

Anna’s hummingbird (Calypte anna; male). What female could resist such gorgeous plumage?

Anna's 1

Anna's 2

Male house finch (Haemorhous mexicanus). They get a lot of their red breast color from carotenoids in the food—as in the photo—and the females are attracted to redder males. Some theorize (and there are supporting data) that the females have evolved this “choice” because redder males are better-fed males, and would make better parents, feeding the young more frequently and, perhaps, being less susceptible to disease or parasites.

Male house finch

 I asked Bruce, since readers like to know technical stuff, what equipment he used to take the pictures. He replied:

I use a Canon digital SLR. The robin and backlit waxwing were taken with a Canon 100-400mm zoom lens, excellent value for the moderate price. The hummingbird, finch and waxwing eating a berry were taken with my new Canon 500mm F4 lens (astonishingly good) with a 1.4 extender added (making the lens a 700mm lens).  I also get extra magnification because my camera does not have full frame sensor camera (yielding a 1.6 magnification crop factor). Altogether, this setup gives me 23 times magnification—like a telescope—completely crazy and it opens up lots of opportunities.

Cedar waxwing (Bombycilla cedrorum), one of my favorite birds because of its crest and cool color pattern:

Cedar waxwing 1

Waxwing 2

American robin (Turdus migratorius):

Robin

And I’ll throw in as lagniappe a photo of a Great Blue Heron (Ardea herodias) by regular contributor Stephen Barnard from Idaho:

Great Blue Heron

Woomeister to give prestigious public-school lecture in UK

January 20, 2014 • 11:14 am

Bedales School, located in the town of Steep in southeast England, is one of the most prestigious “public schools” in the UK. As you know, those are the equivalent of what we in the US would call “private boarding schools,” catering to children (males and females in this case) between about 13 and 18 years old.

The school has an annual “Eckersley Memorial Lectures,” designed to stimulate an interest in science. You can read about some past speakers here (pp. 9-11). Since the lectures began in the Sixties they’ve included a number of scientific luminaries like Herman Bondi, Lewis Wolpert, Colin Blakemore, Ken Pounds and Nobel Laureates Lawrence Bragg and Max Perutz.

Well, look at the luminary they’ve chosen for this year’s lecture:

Picture 1We have Chopra; England has Sheldrake.

It’s outrageous that someone with such wacko ideas is not only being honored this way, but will be given the chance to corrupt young minds with ideas about morphic resonance, psychic phenomena, and How Dogs Know When Their Owners are Coming Home.  And the lecture blurb actually boasts of this stuff, characterizing Sheldrake as “one of the world’s most innovative biologists and writers.”  “Notorious” would be a better word than “innovative.”  Sadly, a bunch of kids in this sold-out lecture will get to hear that materialism is a dying paradigm in science. What were they thinking?

I feel sorry for the lost opportunity to turn kids onto real, genuine, materialistic, hard science rather than fluffy woo. I don’t know about you, but I’m at least going to register a small protest.

Email: admin@bedales.org.uk (the headmaster is Keith Budge)

The Governors of the School can be contacted via Helen McBrown at hmcbrown@bedales.org.uk

Media Enquiries: Please contact Director of External Relations, Rob Reynolds (rreynolds@bedales.org.uk)

One of the school’s mottos is “We grow enquiring minds.”  In this case, they’re going to stunt them.

Newly translated pre-Biblical tablet describes a great flood and a “rescue boat” with wild animals aboard—in pairs!

January 20, 2014 • 7:19 am

We’ve known since at least 1872 that the Great Flood detailed in Genesis is a descendant of earlier flood myths from Mesopotamia.  And there may be some credibility to the presence of at least some serious floods then, based on the fact that Mesopotamia is a giant flood plain and the presence of some archeological evidence for a big flood around 5000 BC. But what we didn’t know until now is that those earlier flood myths also incorporated a boat onto which species of wild animals were sequestered to save them—two by two!  This clearly shows, as if we didn’t know it already, that the Genesis story of Noah and the Ark isn’t true, but was simply an embroidery of earlier flood stories. (It will be interesting to see how Biblical literalists like Ken Ham react to this finding.)

This has all come to light since the recent deciphering of a clay cuneiform tablet first shown to curators at the British Museum in 1985, but not surrendered by its owner for translation until 2009.  Now the remarkable results are detailed in a book by Irving Finkel, Assyriologist and “assistant keeper” of ancient writings at the British Museum. Finkel’s book, The Ark Before Noah: Decoding the Story of the Flood (released in the US on Jan 30, Kindle only;  already available at Amazon UK in hardback, Kindle, and paperback—the last for a tad more than 8 pounds). Finkel’s article (see below) is very well written, so I suspect his book will be a good read.

First, here’s Finkel (he’s Jewish), who bears a remarkable resemblance to both an aged Darwin with more hair, and an even closer resemblance to my friend at UC Davis, Professor Michael Turelli:

irving-finkel-two_2791802b
Irving Finkel (Photo: Benjamin McMahon)

Here’s the “Ark tablet” that Finkel and the British Museum finally got hold of four years ago. It contains 600 cuneiform characters and is dated between 1900 and 1700 BC, which makes it roughly a millennium older than the book of Genesis. According to Finkel, Genesis was assembled between 597 and 538 BC during the Jewish exodus in Babylonia:

ark-tablet_2791738c
The Ark Tablet, which dates from around 1900BC (Benjamin McMahon)

The remarkable story on this cellphone-sized table is detailed in two pieces in yesterday’s Telegraph: an interview with Finkel by science writer Tom Chivers: “Irving Finkel: reader of the lost Ark“, and a piece written by Finkel himself,”Noah’s Ark: The facts behind the flood.” There’s also a very positive review of Finkel’s book by James McConnachie in yesterday’s Sunday Times, but it’s not online (thanks to pyers for scanning it for me). The two Telegraph pieces are must-reads for visitors to this site.

Here’s a quick overview of what’s old and new; quotes from the articles are in italics:

  • We’ve known since 1872, from another cuneiform tablet that came to the British Museum, that there were Mesopotamian flood myths that long antedated the one in Genesis. Other tablets surfaced, and their contents are famously detailed in Tablets XI and XII of the Epic of Gilgamesh, written beginning about 2000 BC.
  • A bit about cuneiform writing: it’s apparently very complicated, with symbols that can stand for either words, syllables, grammatical phrases—and in more than one language.  Finkel has handled so many of these tablets that he’s learned to recognize individual scribes:

Finkel has been doing this for so long, and “met” so many of the same scribes over and over again, that he gets a sense of them as people. The Babylonian schools were filled with the same mix of troublemakers, bored kids and swots as modern ones, he says, which you can tell from the recovered tablets from children learning to read and write. And when you read a really learned, intelligent, experienced scribe, “you can really see a brain there, a brain that’s clever and can see meaning. They were very sharp.”

I ask him if he has any favourites, if any of the writers become almost friends. “You get cleverness and intellect, but what you don’t get, usually, is personal stuff,” he says. “You don’t get private writing, you don’t get spontaneous love poetry. So one is filled with admiration for these minds, and sometimes you wish you could bloody well talk to this guy so he could explain what he means, but not a feeling that you’d like to go for a pint with him or something.”

Occasionally, though, he finds that a scribe has missed a line in a long, copied document, and they’ve tried to squeeze it in in the margin, with an asterisk to mark the spot: “The device is familiar, that’s like us. And it’s that sense of the guy going ‘oh s—’ – that’s the moment you think you might like to buy this guy a pint and calm him down.”

  • The boat described as the earlier Ark was a huge coracle: a shallow round boat made from coiled ropes of palm fiber. Finkel describes it as being 230 feet in diameter (Chivers’s piece says 70 feet, but he must mean meters, since 70 meters is almost exactly 230 feet). The length of palm rope required for such a large boat would, says Finkel, stretch from London to Edinburgh. The new “Ark tablet” is quite detailed about the coracle’s construction:

Before the arrival of the Ark Tablet, hard facts for the boatbuilder were sparse. We have had to wait until now for the statistics of shape, size and dimensions, as well as everything to do with the matter of waterproofing. The information that has now become available could be turned into a printed set of specifications sufficient for any would-be ark-builder today.

Enki tells Atra-hasıs in a very practical way how to get his boat started; he is to draw out a plan of the round boat on the ground. The simplest way to do this would have been with a peg and a long string. The stage is thus set for building the world’s largest coracle, with a base area of 38,750sq ft, and a diameter of, near enough, 230ft. It works out to be the size of a Babylonian “field”, what we would call an acre. The walls, at about 20ft, would effectively inhibit an upright male giraffe from looking over at us.

Atra-hasıs’s coracle was to be made of rope, coiled into a gigantic basket. This rope was made of palm fibre, and vast quantities of it were going to be needed. Coiling the rope and weaving between the rows eventually produces a giant round floppy basket, which is then stiffened with a set of J-shaped wooden ribs. Stanchions, mentioned in lines 15-16, were a crucial element in the Ark’s construction and an innovation in response to Atra-hasıs’s special requirements, for they allow the introduction of an upper deck.

These stanchions could be placed in diverse arrangements; set flat on the interlocked square ends of the ribs, they would facilitate subdivision of the lower floor space into suitable areas for bulky or fatally incompatible animals. One striking peculiarity of Atra-hasıs’s reports is that he doesn’t mention either the deck or the roof explicitly, but within the specifications both deck and roof are implicit. (In line 45 Atra-hasıs goes up to the roof to pray.)

Here is a coracle, in a photo from the 1920s:

coracle-building_2791742c

  • Finkel also notes that the tablet describes the boat as caulked with bitumen. Bitumen, of course, is a petroleum-like product, which is the fossilized and transformed remains of ancient microscopic creatures like diatoms. The Genesis Ark, too, was caulked with petroleum-like material, something that’s overlooked by Biblical literalists. If the earth is only 6000-10,000 years old, where did that caulk come from?
  • But the cool stuff is the two-by-two animals on the coracle. There couldn’t have been many species in a coracle that small, so we need a new science: Mesopotamian Baraminology! Finkel’s finding of the animal story is spellbinding:

At first sight, the very broken lines 51–52 of the Ark Tablet looked unpromising. The surface, if not completely lost, is badly abraded in this part of the tablet. I needed, then, to bring every sophisticated technique of decipherment into play: polishing the magnifying glass, holding it steady, repeatedly moving the tablet under the light to get the slightest shadow of a worn-out wedge or two. Eventually the sign traces in line 51 could be seen to be “and the wild animal[s of the st]ep[pe]”.

What gave me the biggest shock in 44 years of grappling with cuneiform tablets was, however, what came next. My best shot at the first two signs beginning line 52 came up with “sa” and “na”, both incompletely preserved. On looking unhopefully for words beginning “sana” in the Chicago Assyrian Dictionary, I found the following entry and nearly fell off my chair as a result of the words: “sana (or sanâ) adv. Two each, two by two.”

This is a very rare word among all our texts – when the dictionary was published there had only been two occurrences. To me, it is the world’s most beautiful dictionary definition.

For the first time we learn that the Babylonian animals, like those of Noah, went in two by two, a completely unsuspected Babylonian tradition that draws us ever closer to the familiar narrative of the Bible. (Another interesting matter: the Babylonian flood story in cuneiform is 1,000 years older than the Book of Genesis in Hebrew, but reading the two accounts together demonstrates their close, literary relationship. No firm explanation of how this might have really come about has previously been offered, but study of the circumstances in which the Judaeans exiled to Babylon by Nebuchadnezzar II found themselves answers many crucial questions.)

There is a further consideration raised by these two lines in the Ark Tablet: they only mention wild animals. I imagine domestic livestock might well be taken for granted, especially if some of the animals were going to be part of their own food chain.

Well, of course there’s no way they could have fit the world’s 7-million-plus species (in pairs) on either the Genesis ark or a 230-foot-diameter coracle, so of course literalists have to explain where the later species came from. The usual answer is “evolution” from a limited set of “kinds,” but this disguises the fact that evolution was admitted to occur! So what were taken on the Ark were a set “kinds” that split into all the species we know today.  The fruitless study of what the kinds really comprised is the subject of “baraminology,” which I mentioned above. It’s the world’s most useless (and, to a scientist, funniest) area of scholarly “research.”

The upshot is, of course, that the Ark story is fiction, which won’t surprise any of us. But when I debated those creationists in Arizona a while back, they all held firmly to the literalism of the Ark Story, and even had an answer to my question about “where did the pitch come from?” (answer: “We’re not sure that the word is accurately translated from the Hebrew”).

I haven’t done any Googling, but I suspect that Biblical literalists already have an answer to the striking similarity of the Genesis flood account to the Epic of Gilgamesh. Readers who know how they comport these should weigh in below.  But now the literalists have extra work to do: explaining why the Bible, which is the word of God, gives a description of animals boarding the ark two by two (or seven by seven for the “clean” animals), yet that very word of God describes similar (but not identical) things written in cuneiform a thousand years before God spoke. If you’re a fundie, you can say either that the cuneiform story was God’s first word, or that it was wrong in its details, and the Ark story is right. You’re screwed either way.

The solution, of course, is to recognize both documents as myths that probably embroidered real-life but smaller floods occurring thousands of years ago in Mesopotamia.

At any rate, have a look at Finkel’s book. Here’s the cover:

Finkel book

h/t: Matthew Cobb, pyers

Monday: Hili dialogue

January 20, 2014 • 3:30 am
Hili: Did the ancient Greeks adore cats?
A: My knowledge in this field is very limited.
Hili: But you do understand that our hedonism cannot have roots in Christianity?

Photo:Sarah

1546368_10202565865135170_940741611_nIn Polish:
Hili: Czy starożytni Grecy kochali koty?
Ja: Moja wiedza w tej kwestii jest bardzo ograniczona.
Hili: Ale rozumiesz przecież, że nasz sybarytyzm nie może mieć swoich korzeni w chrześcijaństwie.

Charlie and the seals

January 20, 2014 • 2:04 am

By Matthew Cobb

Never mind Attenborough and the gorillas, here’s Charlie and the elephant seal. Irish journalist Charlie Bird was filming in Antarctica when he got very close to two elephant seal juveniles. The result was squeesome and I am very jealous of Charlie. On the other hand, it probably wouldn’t have gone so well with an adult male…

h/t @lecanardnoir