Genetics of Behavior: Fire Ants

ResearchBlogging.orgA common presumption is that behavior is part of phenotype, and since phenotype arises from genotype (plus/minus Reaction Norm), that there can be a study of "behavioral genetics." This is certainly an overstatement (or oversimplification) for organisms with extensive and/or complex neural systems, such as humans and mice. Neural systems probably evolved (not initially, but eventually) to disassociate behavior with the kind of pre-determined micro-management of behavior that a simple gene-behavior link requires. However, in organisms with neural systems the size of the period at the end of this sentence, we often do see cases of allelic variations causing behavioral variation in the whole organism. The study discussed here is an example of this.

Solenopsis invicta, a fire ant, can have colonies with a single reproductive queen (these are called mongyne colonies) or a colony wit multiple reproductive queens (called polygyne colonies).

In mongyne colonies, all individuals have a particular allele for one gene. The gene is General Protein-9 (Gp-9), and the allele is the B-like allele.

Polygyne colonies contain individuals with both the B-like allele and the b-like allele (case matters!). This has led to the suggestion that the presence of b-like is necessary and sufficient for the rise of polygyne colonies.

One overarching reason that this sort of thing is important has to do with the eusocial nature of bee, wasp, and ant colonies. In many ants and bees, and some wasps, reproductive altruistic behavior is seen, in which individuals forgo their own direct reproduction in order to assist a single queen and a handful of males produce a large number of offspring. This behavior can be accounted for by the fact that if individuals act more or less alone to raise offspring, they will have just a few offspring, but if they group together in a colony they can produce zillions of close relatives. Producing more offspring directly (more than competing individuals) increases one's fitness. Contributing to the production of zillions of relatives can also increase one's fitness. The idea is that a colonial system allows for greater fitness, indirectly, for non reproductive workers than working alone would.

Bees ants and wasps have a genetic system that also results in this interesting fact: From the point of view of a given female, she (the female) is more closely related to a sister than to a daughter. Therefore, contribution to the production of sisters adds up, in terms of fitness, faster than one might expect.

However, indirect fitness (one's contribution to the production of relatives that re not offspring) if the members of the colony that one is supporting are less related, as would be the case with multiple queens. So why are there ever multiple queens? You can see why this is an interesting question.

There are many species of fire ants, but the monogyne-polygyne polymorphism studied in this paper occurs in only six species in a single clade.

The GP-9 gene codes for a protein that is one of may different proteins that are used as olfactory cues, for communication among ants. It may be the case that this gene relates to the communication that happens between prospective queens and workers, in the process of negotiating which queens will be allowed in a colony (the queens require care and feeding by the workers, so the workers determine the number of queens).

The present study looked at a much larger set of data than previously examined, and confirmed the relationship between b-like alleles and multiple females, but also uncovered important nuances.

...our determination of the social organization of key colonies confirmed the invariant link between the presence of typical b-like alleles and [multiple queens], while our discovery of several novel alleles bearing various combinations of b-like and B-like codons revealed that no single amino acid residue is completely predictive of polygyne behavior.

Where b-like alleles (and multiple queens) occur, one may postulate that there is reduced selection against multiple queens, or increased selection for them. The genetic analysis done here attempts to characterize the selection pattern on this gene. While far from conclusive, the researchers suggest that it is more likely that the presence of b-like alleles causing multiple queen colonies is not so much the result of lack of selection against this, but rather, positive selection for the multiple-queen alleles.

This elevated coding-region variation may result from a lack of negative selection acting to constrain amino acid replacements over much of the protein, different mutation rates or biases in coding and non-coding sequences, negative selection acting with greater strength on non-coding than coding regions, and/or positive selection acting on the protein. Formal selection analyses provide evidence that the latter force played an important role in the basal b-like lineages coincident with the emergence of polygyny.

I am left wondering what the selection force for multiple queens would be, and would like to see the author's speculation in this area.

Gotzek, D., Shoemaker, D.D., Ross, K.G., West, S. (2007). Molecular Variation at a Candidate Gene Implicated in the Regulation of Fire Ant Social Behavior. PLoS ONE, 2(11), e1088. DOI: 10.1371/journal.pone.0001088

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Now how about a post on how to kill fire ants?

I am generally non-violent, and even try to carry spiders out of the house or sweep out a roach rather than kill them, but fire ants have become the enemy. They attack people who are innocently gardening or children who pick up a toy left outside for a few hours. They spread so rapidly that they can quickly make a yard all but unusable.

When I was a child, I would lie in the grass and watch the clouds go by. Now that same grass is so full of fire ants that I have to make my grandchildren play on the paved driveway. The poisons readily available kill butterflies, sometimes injure birds, and wash into the nearby wetlands to kill dragonflies and small fish.

I've tried vinegar, hot water, and dishwashing detergent. They all help a little, but are extremely labor intensive to apply and do their own damage to surrounding vegetation and insect life.

The person who eventually finds an affordable way to get rid of fire ants without doing in all the nearby living things is going to be very rich I think. Maybe a way to affect their genes so that they build mounds as though protecting a queen but in fact without a queen or with a queen that can't reproduce?

As far as the adaptive advantage of the polygyne colonies, I'll try to remember back to the departmental seminars.

I believe the working hypothesis is that polygyne colonies are bigger and can colonize new territories faster. This will be adaptive as long as fire ants' range is expanding.

I'll send the lead author a note to drop in.

Hi Greg,
glad to see that someone is actually reading our papers. ;) You raise a good question and honestly, as you mention, at this point we can only speculate.

Within colonies, it seems clear that Gp-9 (or the locus/region that it marks) is a selfish element and workers (of which a sufficiently large percentage must also carry the b-like allele) only allow b-like bearing queens to reproduce.

At the colony level things are a lot less clear and we only have some anecdotal evidence from the introduced North American range and unfortunately know nothing about what goes on in the native range in South America. Reed has given part of the answer above (again I'm glad to see that someone paid attention during seminars). As far as we know, there are no known ecological differences between the two forms and they occupy identical niches. It seems that polygyne colonies can simply outcompete monogyne colonies since they form much larger colonies and are not aggressive towards other polygyne colonies. Monogyne colonies on the other hand are highly territorial and aggressive towards non-nest mates. There are reports that the two can co-occur for prolonged periods of time although it is not clear whether the monogyne colonies in these situations are established colonies, capable of holding their own against the polygyne form, or whether they are newly established and can only persist transiently. At least in the study populations around Athens, GA, the polygyne form has almost completely displaced the monogyne form, with the latter only holding on in small pockets here and there. Clearly a lot more work is needed in this area... :)


By Dietrich Gotzek (not verified) on 25 Mar 2008 #permalink

This reminds me of killifish, in a roundabout way. Normally killifish are obligate internally self-fertilizing hermaphrodites. Males are occasionally born, but they don't get to play the reproduction game.

However, there are populations of killifish for which sexual reproduction has been observed between males and "females" (immature hermaphrodites). Since these sexually-reproducing populations correlate with geologically young environments, it is speculated that sexual reproduction is induced as a mechanism for generating diversity for adaptation.