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August 31, 2010

There's much more to Hamilton's rule than haplodiploidy

Updated 27 October 2010: Evidence for kin selection's role in the evolution of eusociality in insects includes ancestral-state reconstruction showing that all eusocial species are descended from ancestors with monogamous queens, which increased within-colony relatedness. See this earlier post.

A recent paper in Nature, challenging an obsolete explanation for the evolution of eusociality (characterized by nonreproductive individuals, like worker bees), may be misinterpreted as evidence against Hamilton's rule.

Hamilton's rule, you may recall, is that alleles (gene variants) for altruistic behavior (increasing another's fitness in ways that reduce one's own) will spread if, on average:
c < b r
that is, if the fitness cost to the altruist is less than the fitness benefit to the recipient, times the extent to which the recipient is more likely (relative to the population with which they compete) to have the same altruism allele. Often, this increased likelihood of sharing the same gene is due to genetic relatedness.

The haplodiploid genetic system used by ants and bees means that a worker can be more likely to share alleles with her sisters (r=0.75, relative to unrelated individuals) than with her own offspring (r=0.5). It was once suggested that this could explain why worker ants care for their sisters (the queen's daughters) rather than having offspring of their own. But then someone pointed out that Hamilton's r between a sister and a brother is only 0.25. So, if the queen has equal numbers of sons and daughters, there's no reason for workers to favor siblings over their own offspring. The central point in this new paper, that haplodiploidy doesn't necessarily lead to eusociality, is therefore both consistent with Hamilton's rule and old news.

I'm not sure how long we've known this, but The Selfish Gene, published more than 30 years ago, mentions the low Hamilton's r of 0.25 for brothers and focuses, not on any link between haplodiploidy and eusociality, but rather on conflict between workers and queen over the sex ratio of the latter's offspring. In particular, Dawkins discussed work by Trivers and Hare, who used Hamilton's rule to predict a 3:1 female:male ratio in most ants but a 1:1 ratio in slave-making species, predictions that were confirmed by field observations.

Carl ZImmer's discussion of this paper in the New York Times includes comments from Andy Gardner, a leading evolutionary theorist:

"This is a really terrible article." One problem Dr. Gardner points to is the Harvard team's claim that the past 40 years of research on inclusive fitness has yielded nothing but "hypothetical explanations."
"This claim is just patently wrong," Dr. Gardner said. He points to the question of how many sons and daughters mothers produce among the many insights inclusive fitness has brought.

Jerry Coyne (author of Why Evolution is True) didn't like the paper either.
Nor did Richard Dawkins.
Or Jeremy Joder.

August 27, 2010


Here are some papers that look interesting this week:

Signal diffusion and the mitigation of social exploitation in pneumococcal competence signalling


Caloric restriction or catalase inactivation extends yeast chronological lifespan by inducing H2O2 and superoxide dismutase activity


Evidence for competition between carnivorous plants and spiders


Paleoclimate and bubonic plague: a forewarning of future risk?

August 24, 2010

Another way to alarm aphids



August 20, 2010

Local food?

This blog makes some important points, as do some of the comments.

August 19, 2010

Evolution-proof pest-resistant crops?




The first generation of aphids on the false-alarm plants were often repelled by them, and also reproduced less. Maybe they were feeling stressed. But the second and third generations were about 50% and 25% as likely to be repelled.

So far, this looks like another example of pests quickly evolving resistance to our pest-control measures. But the alarm-ignoring aphids were twice as likely to get eaten by predators. Normally, they would detect alarm signals when other aphids nearby get eaten, and fly away or drop off the plant, escaping the predators. Ignoring the false-alarm from the plant "crying wolf" increased their chances of getting eaten. So maybe this approach would be relatively evolution-proof.

(I suggested as much in the draft of my book, "Darwinian agriculture: where does Nature's wisdom lie?" which I'll now have to revise to include this interesting paper. So far, Princeton University Press has sent me one detailed and positive review and one sketchy and negative review. They need another review, so the book will be delayed a bit.).

So what happened from generation 1 to generation 3? The authors don't think it was evolution (i.e., a change in the genetic composition of the population) because it happened to fast and because they could reverse the effect with three generations on plants that didn't make false alarm signals. I'm not so sure. With strong selection and some genetic variability in the population, changes at least as big as they found can certainly evolve.

They found changes in gene expression, but I don't see how that answers the question. An evolutionary change will usually lead to differences in gene expression, but you can also get differences in gene expression without evolution.

Two unusual features of aphids are (1) that they usually reproduce by parthenogenesis, with females giving birth, without sex, to daughters genetically identical to themselves (apart from any mutations) and (2) that adult females already contain tiny daughters and granddaughters. So here are two possible explanations for the changes observed:

1) Evolution. One member of the first generation had a mutation making her ignore alarm signals. Since responding to false alarm signals reproduces reproduction, she had more daughters and granddaughters than the others, increasing the frequency of alarm-ignoring genes in the population.

2) "Maternal effects." There are many examples of the environment to which a mother animal or plant is exposed affecting their offspring. Sometimes this involves some modification of their DNA, such as by methylation (see "epigenetics"). (The authors use the term "habituation", which I think it usually refers to a behavioral change in an individual, rather than a change over generations.)

Maternal effects aren't always beneficial, but they were in this case. Is this just chance, or did this tendency of daughters and granddaughters to ignore alarm signals if their mother or grandmother were exposed to false alarm signals evolve? Such responses rarely evolve "because they might be useful in the future" -- they must have been useful in the past. I would only expect such maternal effects to evolve if responding to alarm signals was sometimes beneficial and sometimes harmful over the evolutionary history of this species, and if conditions to which the mother was exposed were a consistently good predictor of the response that would be most beneficial to the daughter. This isn't impossible, but I wouldn't rule out the simpler alternative that the populations under study evolved over three generations. Maybe the authors have additional data that would disprove this, however.

It's also worth mentioning that parthenogenesis leads to clusters of genetically identical aphids. This genetic uniformity makes cooperation evolve more easily (e.g., alarm signals to warn others nearby when you're being eaten) than if these were aphids of different genotypes competing for resources.


Our paper showing that delaying reproduction can increase fitness (when environmental cues predict population decline) was apparently the most-viewed story on the University of Minnesota website.