Long live our queen, the parasite

Ant Day, like so many cherished holidays of my youth, has come and passed. We spent the day bushwhacking through Pipeline Road with myrmecologists Andy Suarez and Corrie Moreau, and then excavated some leafcutter nests with Hubi Herz to extract queens, fungal gardens, and have a look at nest architecture (while destroying the yard of a certain STRI researcher). Hopefully, some photos will circulate our flickr in the near future (though I can’t take responsibility for any of them). Check ’em out, a deer got involved. The only comment I’ll make on the actual field work is that collecting ants and digging up nests is utterly exciting, like the best scavenger hunt you’ve ever been on. This is how all biology used to be, inclusive to the point that anyone could get involved by just walking outside and looking around. Let’s blame James Watson and call it a day.

This blog post pertains to the origin(s) of eusociality, so here’s a quick disclaimer: I don’t subscribe to one theory, and I generally oppose anything that polarizes folks with as much acrimony as we’ve seen in the past few years after the Nowak et al. paper that redacted kin selection. Sure, I’ve always looked at Hamilton’s famous inequality with healthy skepticism, but that may simply be because there’s math involved. If this paragraph hasn’t made sense so far, here’s a quick review of eusociality and some major explanations that are on the table, after which I’ll bring up a new idea, imparted unto me on this very special day.

I think I eschew defining an always-applicable set of rules preempting eusociality, taking more of an “I know it when I see it” approach, with the caveat that there are definitely some key features upon which we can all agree. The three basic pre-requisties are: overlapping generations (queens and daughters operate side-by-side), cooperative brood care, and division of labor. Humans pretty much meet these conditions, but what separates boring old human interaction from the extreme communism of the insect societies is reproductive altruism; that is, workers, who retain the original plumbing required to reproduce, have almost no reproductive potential. This feature puzzled Darwin, as it challenged the very idea that all organisms should operate in a way that maximizes their fitness, or the likelihood that they’ll pass on their genes to the next generation. In light of natural selection, how could sterility ever be selected for?

The ongoing war is between two major theories: kin selection and group selection. Kin selection invokes Hamilton’s rule that predicts self-sacrificing behavior if it increases one’s inclusive fitness; that is, the probability of one’s genes being passed on indirectly, like through a sister or a brother (you do share half your genome with your siblings, after all). Because of haplodiploid sex determination, which is seen in many eusocial societies (but not all!), sisters are more closely related to each other than they are to their mothers and/or potential daughters. Therefore, having more sisters, rather than having children, is the more efficient way to make sure your genes are better spread around. Group selection is pretty self-explanatory and encompasses all eusocial societies, predicting that living in groups is selected for for some obvious reasons, like strength in numbers. The queen is an ovary: protect her, protect the genome, protect the lineage.

Like I said, I don’t think one is the absolute truth. On Ant Day, I learned about a new possibility. Andy brought up an idea that really interested me, adding to an arsenal of potential explanations for the repeated emergence of eusociality. Apparently, Robert Trivers, in between developing parental investment theories and attending Black Panther meetings, introduced and quickly abandoned the notion that worker sterility as maintained by queen presence (via pheromonal “blocking” of ovariole development, for example) is an example of queen parasitism. That is to say: queens parasitize their daughters, which double as hosts, eliminating their reproductive potential so she can wallow in the joys of motherhood while her daughters do the heavy lifting. I can’t find too much written on this, but I think the general idea is that workers, unable to reproduce, either die alone or stick around and benefit from inclusive fitness effects. With this model, there’s no altruism, and every selfless action that appears to be “for the good of whole” ultimately stems from victimization of the non-queen castes. You are thinking: this is the least romantic of the explanations. In honey bees, if the queen dies (long live the queen) and a new queen can’t be raised, worker ovarioles develops and at least a few workers will gracelessly start laying eggs. Because their eggs can only produce males (recall: haplodiploidy!), their colony is doomed and their laying is a blitz to send out half their genome with the hopes that a new colony can be founded. Or is this just what they’re like in solitary state, without their queen, the parasite?

Watching leafcutter trails and army ant swarms, the coordination of action is overwhelming. Everyone just “knows” what to do, and carries out a caste-specific task in an unquestioning, stereotyped manner. To think all of this is orchestrated by antagonistic interaction is an incredible premise, one that I hope to explore and possibly test in the future. If it is the case, then eusocial societies are the most fantastic exercises in population control.

Thoughts welcome.

ian

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