There’s a new paper in the Proceedings of the National Academy of Sciences USA by David A. Galbraith et al. (free link and reference at bottom) that has a very cool result: one predicted by kin-selection theory. Kin selection, as you may know, is the idea that the adaptive value of a gene (and hence its evolutionary fate) must include information about how that gene affects its copies in relatives (e.g., a gene in parents for taking care of offspring can promote the replication of the copies that also occur in those offspring). Wikipedia describes this idea pretty succinctly.
Kin selection has been a very useful concept in understanding things like behaviors directed at offspring and relatives, and particularly in understanding the evolution of altruism and of one of its forms: eusociality—the behavior in which a colony of individuals is divided up into castes, some of which reproduce and some of which are nonreproductive but tend the “queen’s” brood (honeybees and naked mole rats are examples).
There are a few people, though, most notably Martin Nowak and E. O. Wilson at Harvard, who have questioned the usefulness of kin selection, arguing that group selection theory (or “multilevel” selection theory) is the only way to study the evolution of eusociality. I’ve written a lot on this site questioning their ideas (see some links below) as well as their claim that kin selection is not a useful way to study evolution in nature. The paper below, I think, shows the usefulness of the kin-selection paradigm, which seems to make predictions—ones that are verified—that don’t flow in any obvious way from a perspective of group or multilevel selection.
Because the paper is complex, I’ve asked my friend Phil Ward, a professor of entomology at the University of California at Davis (and a student of insect evolution) to explain its predictions and results. His explanation may be a bit difficult for non-biologists, but there is no simpler way to explain the study. Give it a go!
by Phil Ward
There has been a vociferous debate over the relative merits of group selection theory and inclusive fitness theory (or kin selection theory) as explanations for the evolution of altruistic behavior, especially following a contentious paper by Nowak et al. (2010) which claimed the superiority of the group selection approach. This was met with a resounding rebuff by a large group of evolutionary biologists who argued for the much greater explanatory power and heuristic value of inclusive-fitness thinking (e.g., Abbot et al. 2011). Some previous postings on WEIT about this topic have appeared here, here, here and here.
One fruitful area of inquiry in which kin selection theory makes explicit and testable predictions is in the study of genomic imprinting, a form of intragenomic conflict in which there is differential expression of genes inherited from the mother versus the father. In a theory paper published more than a decade ago, David Queller pointed out that this form of intragenomic conflict can be expected to be particularly widespread in colonies of social insects, and he employed kinship theory to predict the outcome of such conflict under different social contexts.
Now a recent empirical paper by Galbraith et al. (2016) provides convincing evidence that intragenomic conflict in honey bees indeed reveals itself in a way predicted by kin selection theory.
The authors first point out that genes inherited from mothers (matrigenes) and those inherited from fathers (patrigenes) are expected to be in conflict in honey bee workers that have an opportunity to reproduce. Why? Because a honey bee queen mates with multiple males, and the resulting workers are mostly half-siblings. These half-sibling individuals share half of their matrigenes but none of their patrigenes (see Figure 1 of the paper). So, consider a colony in which the queen has died, and half-sibling workers begin to compete over egg-laying (this behavior is inhibited by the queen while she is still alive). A worker’s matrigenes can be passed on when either she or her siblings reproduce, but her patrigenes are present only in her own offspring. Hence, as the authors put it, “compared with matrigenes, patrigenes will favor worker reproduction and exhibit enhanced activity on worker reproductive traits”.
This prediction was tested by quantifying the extent of genomic imprinting, i.e., the differential expression of genes of paternal origin.
The authors’ predictions were upheld. Using a series of genetic crosses that allowed them to distinguish matrigenes from patrigenes, they found that workers in queenless honey bee colonies showed greater expression of paternal than maternal genes, and this patrigene-biased expression was even higher in those workers that actually reproduced. In addition, when comparing parent-of-origin effects on reproductive traits such as ovary size and ovarian activity, patrigenes were shown to exert a much greater influence than matrigenes.
It should be emphasized that the worker reproduction occurring in queenless honey bee colonies produces only one sex: males.The workers lay unfertilized eggs and, as a consequence of the peculiar genetic system (haplodiploidy) found in bees, wasp and ants, these haploid eggs develop into males (which thus carry only one set of chromosomes). With no further production of workers, the colony will soon decline.
So, this last gasp of haploid reproductive effort that occurs when a queen dies (and is not replaced) will have selective significance only if the males that are produced have an opportunity to mate with queens from other colonies, something that takes place in population-wide mating swarms. Presumably this process of rearing and releasing drones (male bees) in a timely manner works best if some workers reproduce while the remainder continue to forage for food and feed the developing drone brood. Thus, colonies in which all reproductively capable workers give in to their patrigenic impulses might produce fewer reproductively successful drones than those in which there is some degree of reproductive restraint by the workers. One could argue that this is a kind of “colony-level” selection that weeds out disruptively high levels of patrigene expression, but inclusive fitness theory would explain this as a consequence of cost-benefit ratios that moderate the expression of both matrigenes and patrigenes.
Finally, for the small fraction of workers in a honey bee colony that are full siblings, the genetic interests of matrigenes and patrigenes are quite different: patrigenes can be equally well propagated through a worker’s own reproduction or that of a full sibling. Most competition for reproduction in honey bees is among half-siblings, however, so this should have little effect in honey bee colonies. Nevertheless, among other social insects in which the queen mates only once (such as bumble bees and many species of ants) all workers are full siblings and, as the authors note, the prediction is reversed: matrigenes should favor worker reproduction and show enhanced gene expression relative to patrigenes. Apparently this has not yet been studied, but it would constitute an elegant complementary test to the ground-breaking results of Galbraith et al.
, D. A., S. D. Kocher, T. Glenn, I. Albert, G. J. Hunt, J. E. Strassmann, D. C. Queller, and C. M. Grozinger. 2016. Testing the kinship theory of intragenomic conflict in honey bees (Apis mellifera). Proc Nat. Acad Sci. USA 113:1020-1025. doi:10.1073/pnas.1516636113