A Queen's Choices
Tipping the odds just a little
Life’s many intersections present us with choices, and our decisions, in the words of Robert Frost, “can make all the difference.” Many choices are obviously Very Important, with far-reaching consequences---marriage, job, children, home, and so on. It is less obvious that our lives are also shaped by thousands of other choices, events that barely rise to the level of consciousness, but can shape our future, nevertheless. Most of these choices and events seem so inconsequential that we do not even include them in our life’s narrative. As a student of the life histories of ants, I sometimes contrast our narratives with those of ants and have come to appreciate how much life within a cushioning society has made human choices so much less dangerous, so much less lethal. Early in their lives, ant queens also enjoy such a social cushion, but unlike humans whose entire lives are spent within societies, those of ant queens are exposed to the rawness and lethality of solo life during colony reproduction.
To illustrate this fact, I will describe the life of a fire ant queen within the society that produced her, followed by the solo phase when she tries to start a new colony alone, without the safe mantle of the colony. This comparison shows the value of sociality for getting through life in one piece, both for the fire ant and for us. Like people, fire ant queens begin their lives in a colony, a highly protective family of sisters, one that functions like an organism of organisms (hence the name superorganism). Just as organisms recap their evolutionary history during reproduction by reverting to their single cell ancestral conditions (eggs and sperm), so do superorganisms revert to their solitary ancestry (the winged sexual female and males) during superorganismal reproduction.
Our queen was one of about 1000 that hatched that year in a large fire ant colony. Her larval life was one of continuous pampering, with a nurse worker checking every few minutes to ask, Are you hungry, dear? And then to feed her a nutritious snack if the answer was Yes! As a queen-destined larva, she was fed far more frequently than worker larvae and as a result, she grew to several times their size, and developed ovaries and wings. Just as a human child has a very high chance of survival to maturity, so does our queen, thanks to the protection of her parent society. Even after she emerges as an adult sexual, the colony feeds her to the bursting, and after two weeks, half of her body weight is fat, metabolic stores that will allow her to start a colony alone and without feeding.
Despite her well-protected upbringing, our queen’s social cocoon vanished in an instant when she, along with hundreds of her sisters and brothers took flight in the crucial event for which the colony had produced her--- colony reproduction, the founding of a new superorganism. This complex, fraught process is heavily dominated by chance and factors not under the queen’s control, but over evolutionary time, she has come to respond to the many choices she makes so that they nudge fate a tiny amount in her favor. From the outset, her chances of success are minuscule, yet she struggles mightily, applying the blunt tools that evolution has given her, and gathering local information to make the choices she must.
On the day of the mating flight, our queen leaves the nest mound through large holes the workers have made, climbs up on vegetation and takes flight. As she rises into the sky, she must escape becoming a snack for cruising dragonflies and birds. Once aloft, she enters a thin layer-swarm of fire ant males that have been cruising back and forth for about half an hour, waiting for her. She mates with one in mid-air, receiving a package of about 7 million sperm that she stores in a little sac connected to her genital tract. This is her lifetime supply, for she will never mate again.
After mating, she descends toward the ground and faces her first crucial choice: where should she land? She can stay airborne for an hour or two during which she traverses and evaluates the habitat rolling beneath her feet. She would prefer a large, barren patch, but she cannot fly indefinitely and will settle for less--- a smaller bare patch, partly vegetated and disturbed, or at least not shady. If, after landing she finds the spot too inhospitable, she can choose to take flight again to seek a more congenial spot. As with everything she does, both staying and leaving come with risks. Having accepted a spot as suitable, she swings a leg over her wings and, one by one, breaks them off, grounding her for the remainder of her life. Her travels are now limited to a few meters as she searches for an exact spot at which to start digging her founding nest.
She must dig herself to safety quickly, for on the surface, she is a sitting duck (sitting ant?) for everything from ground beetles to spiders to sparrows. Any preformed hole promises such escape, but if she does not find a suitable one soon, she chooses to dig where there is a slight elevation, thereby reducing the chance of future flooding. Once the burrow is a few centimeters deep, she plugs the opening from below, sealing herself in and over the next few days, lays up to 50 eggs produced from her metabolic reserve. About half of these lack a nucleus and are food for the developing larvae (ant omelets). Some of her “choices” in this phase may seem more like physiology, but they are crucial, nevertheless. Topping the list is how much of her stored reserve to invest in offspring, and how much to keep in reserve to keep her alive after the new workers have emerged. Queens vary enormously in this proportion, suggesting that it may be an active choice.
Under favorable conditions, the mating flights of thousands of fire ant colonies are synchronized by rain, each releasing hundreds to thousands of sexuals. By mid-afternoon, every desirable square meter of ground may contain multiple mated queens searching for a nest site. Every one of these is on the quest to become the one and only queen of the future colony that will eventually claim a territory of perhaps 100 square meters, often pressed against ant neighbors in all direction. All the other queens will die sooner or later. Facing such odds, the best our queen can do is to nudge fate ever so slightly in her favor, choice by choice, based on local, just-in-time information, but none assure success.
As our queen searches for a place to dig a founding nest, she encounters other queens doing the same thing. The queens often line up like dogs and sniff each other’s rear end. What they learn from this is unknown, but if the queen could keep count of such meetings, she would have an index of how strong her future competition would be. Could she “plan” for this future competition? Indeed, she can! She has a choice of starting the colony by herself, or joining another queen (or more than one) to cooperate in founding a colony. The likelihood of sharing a burrow increases as the density of queens and burrows increases, increasing the opportunities for joining other queens. After very large mating flights, burrows can contain up to five or ten newly mated queens.
A queen that chooses to share a nest can still change her mind before the nest is sealed, and continue her search or dig her own nest. How do queens decide whether to join other queens? Robust queens are more likely to join queens that are also robust, a possible nudge for nest survival. What if a queen finds herself in an unfavorable group? Can she switch, even though the nest is sealed? Yes, she can open the plug and search the area for other nests to try to dig into. Whether this improves a queen’s chances is unknown, but because it happens, it may.
With the nest entrance sealed from below, these queens now begin to lay eggs, initially all at the same rate so that the number of eggs is simply a multiple of the number of queens. Recall that half the eggs are food for the growing larvae. As the founding period wears on, a repeated count of the larvae reveals that the number of larvae per queen declines with group size and with time, even though the initial number of eggs each queen laid was similar. Larvae disappear without a trace, most likely eaten by the queens. Many of the queens that die are also eaten by the surviving queens, but there is no evidence that queens kill one another.
Why would queens eat their brood, when the number of workers they produce is tightly related to their future success? The reason is that the queens are gambling on the success of two conflicting goals at the same time--- the success of the nest, and their own, individual success. These two are linked in complex ways and reveal the subtlety of the gambling involved. First, the success of the communal nest depends on producing more workers, and each queen contributes to this. However, the success of each individual queen conflicts with this communal goal because each queen needs to reserve or accumulate some resources for the next phase of founding in which the queens compete with one another, and a queen’s robustness tips the outcome slightly in her favor (as we shall see). Thus, queens cannibalize the developing larvae to stock their own reserves or to deplete them less. There is no evidence that queens preferentially cannibalize the larvae of the other queens, but in any case, this is a tricky game--- each cannibalized larva strengthens the queen for the post-founding competition but weakens the success of the group.
There must be an optimum between threatening nest survival and serving individual success. Larva production per queen decreases steadily with group size such that total brood is maximal in groups of four. Larger groups are less successful, and most groups of ten or more do not succeed in rearing any brood to the pupal stage. In a real sense, in large groups selfishness overwhelms altruism. At the end of brood rearing, there is a great variation in the amount of weight each queen has lost (or regained through cannibalism), and that weight loss represents her investment in group vs. individual success. As in every group, there can be only so many freeloaders before the group fails.
At the end of the brood rearing period, whether the queen is solo or in a group, the little workers (aka minim workers, or nanitics) open the nest to the surface and explore the surroundings for other recently opened (incipient) nests. If they find other such nests, they simply stroll into them, meeting almost no resistance beyond a brief challenge. They then heft a pupa (preferred) or a larva and carry it back to their own nest, having laid an odor trail to mark the way. But all the minims in the area, including the victims of the theft are similarly engaged, so a mutual brood-stealing contest (aka brood raiding) takes shape. It is common to see a pupa being carried into a nest, and only seconds later, to see it carried back to its nest of origin. These contests can go on for days and involve many colonies (one went for 30 days and 80 nests, but most involve two to five nests and less than 5 days). Eventually one of the nests is declared the winner by means unknown, and the workers deposit all the brood as well as themselves in the winning nest. This means most of the workers have abandoned their own mothers, whose fate without them is grim. It also means that one nest gets a sudden boost in population, a boost that helps it win future such brood raids. The bigger the size difference between nests, the more likely the larger one will win.
Is this a case of evolution going bonkers? Abandoning one’s mother and working for the opposition would not seem to perpetuate one’s germ-line and should not evolve. But it has, so what’s the catch? It is this… when we mark colony founding queens at the beginning of nesting and excavate their nests after the brood raids are done, we find many queens pining alone in empty nests, but we also find some of the marked queens in nests that won the brood raids. Indeed, this shows that some losing queens are not passive, but leave their nests, follow the raiding odor trail, and try to enter the winning nest. If less than 16 hrs. have elapsed, and her daughters are members of that nest, she has a good chance of being allowed to enter. “Abandoning Mom” thus makes a bit of sense, and is another move in the game of odds.
Should she enter, she will participate in an on-going queen-queen competition, a competition in which the workers kill and dismember the losing queens, one by one. These executions take place away from the brood pile, so the once peaceful queens fight, often violently, for a place on the brood pile. Now the earlier cannibalism may pay off, for the more robust, healthier queens tend to win the pile. Being queen-of-the-pile probably compounds her advantage because secretions from older larvae stimulate fertility in the queen, and fertility works in her favor. Perhaps strangely, execution is not based on relatedness, and workers are equally likely to execute their own mother as others.
Many times, these contests go on while the workers are still raiding neighboring nests for brood and abandoned queens are still trying to gain access. In other words, the contest is fluid and shifting, involving many nests and many queens, and the site of the most intense contests can shift to different nests. Eventually and suddenly, workers in these incipient nests switch from tolerating workers from other nests to attacking them as enemies--- the nest thus becomes territorial. The former brood raiding trails often define the nascent territory.
This phase ends when the minims have winnowed all the queens to one. Their numbering system seems to consist of only two numbers--- more than one, and one. From now on, the single surviving queen is the sole reproductrix even though many or most of the minims are not her daughters. All the eggs she now lays are her daughters and will be reared by the worker force. This system is an example of true slavery in the animal kingdom, for the minims are rearing offspring that are of the same species but are not related to them. However, as these unrelated minims gradually die off, the colony consists only of the daughters of the winning queen, a simple family.
At this point, depending on whether our queen attempted founding in empty or ant-occupied territory. Our queen landed in ant-free habitat and is among the 1 to 3% that survived the mating flight and got as far as attempting to found a nest. The extreme level of mortality implies very strong natural selection, selection that has produced the many complex, precise, and special adaptations just described. We see that the queen is not a passive player that relies strictly on luck. In each situation, she makes choices that tilt the odds slightly in her favor. At no time does a choice, or a sequence of choices, result in certainty. Information is always in short supply and the future is unpredictable. Her choices, along with an enormous amount of luck, might place her among the few surviving queens, and evolution has taken note of what it took to do so.
Are her troubles now over so she can lay her eggs in peace? Not yet, and perhaps never. As the many tiny, now single-queen colonies in the neighborhood begin to grow, they come into contact and compete and fight for the same territory. Now the rate of worker production and colony growth take the stage front, for superoganismal territories are all around and territorial gains come from fielding a higher density of workers to push the boundaries against neighbors. Smaller colonies are more likely to succumb to this competition, so that in previously ant-free ground only 0.1% of the queens end up as the mother of a mature colony. If she attempted founding in areas already occupied by fire ant colonies, her chances are only 0.007%.
In the drama of life, fire ants show us the luck and will it takes simply to persist. They also show us in numbers large and small, the value of sociality in that persistence.
This essay is remarkable, and not only for the fascinating and gripping detail in which it explains the challenges and tactics involving newly mated queens. It also leaves this reader in awe of the level of scientific inquiry that must have been required to expose these wonders. Beautiful work!
This chain of events never ceases to amaze me. I often describe this gauntlet when folks underestimate just how complex the lives of little animals can be.