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June 30, 2008

Celebrating ignorance with Sherlock Holmes

We know that some political and religious leaders are proud of their ignorance of evolution, global warming, etc., but did you know that this tradition goes back to Sherlock Holmes? In A Study in Scarlet, he expresses the opinion that it makes no practical difference whether the sun orbits the earth or vice versa. Yet, in The Musgrave Ritual, it turns out that incorrect theories make incorrect predictions...

Holmes: "I looked up at the sun. It was low in the heavens, and I calculated that in less than an hour it would lie just above the topmost branches of the old oak. One condition mentioned in the Ritual would then be fulfilled. And the shadow of the elm must mean the farther end of the shadow, otherwise the trunk would have been chosen as the guide. I had, then, to find where the far end of the shadow would fall when the sun was just clear of the oak."

Watson: I imagine both trees must have grown since the Musgrave Ritual was written, but what do you mean when you say that the sun was "just above the branches" of the oak?

Homes: I suppose it must be a mile or so up to clear the mountains, but I could still tell that it was directly over the oak.

Watson: Do you remember me telling you that the earth goes around the sun? You said you would try to forget it, to leave room in your brain for more important facts.

Holmes: And so I have.

Watson: But the orbit is such that the sun is never directly overhead anywhere in England!

Homes: From where I was standing, it looked like it was right over the oak. So then I just had to locate the far end of the shadow from the elm....

Watson: But surely you've noticed that where the shadow of a tree falls varies with the day of the year, not just with the hour of the day? This is a direct consequence of the orbital pattern you were so eager to forget.

Holmes: It's good that I have you to keep track of such minor details. I hadn't noticed.

Watson: You saw, but you did not observe.

June 29, 2008

Evolution 2008: sexy plants, battling bacteria, durable cooperation

About 1500 scientists attended Evolution 2008 here last week. The four-day meeting was filled with 15-minute talks (usually ten at once, in different rooms), plus two evening poster sessions (like a science fair, for grownups, with discussions rather than judging), scenically located on a pedestrian bridge over the Mississippi. Reports that "scientists are abandoning evolution" appear to be exaggerated.

Here are summaries of some of the talks I enjoyed.

Sexy plants

It has been suggested that harsh environments may select against elaborate sexual displays. For example, peacocks with fancier tails may mate more often (but see last week's guest post), increasing the frequency of fancy-tail genes in the population. But if predators are very common, the increased risk of being eaten may outweigh sexual selection. OK, but why worry about animals, when plants are so much more interesting?
Chris Herlihy talked at Evolution 2008 about a plant that lures pollinators with elaborate clusters of male flowers. Male plants with more flowers attract more pollinators, but the flower clusters also have lots of small, thin leaves, which lose more water, increasing the risk of death during a drought.

Herlihy and Lynda Delph imposed selection, under greenhouse conditions, for more elaborate male flower clusters, analogous to what would be imposed by choosy pollinators) and found that they evolved readily. Given plenty of water, lines selected for more elaborate flower clusters made more pollen and would presumably attract more pollinators, achieving more male reproductive success.

Herlihy also mentioned some related field experiments. Lines selected for more elaborate flower clusters were more likely to die in the field, apparently due to their greater water use. They saw a similar pattern in wild plants, not subject to artificial selection, in the field. Males with more flowers were more likely to die at dry sites, whereas at wet sites they survived well and presumably had more offspring than plants with fewer flowers. These observations were consistent with the hypothesis that, for plants as well as animals, the cost of elaborate male displays is more of a constraint in harsh environments.

Battling bacteria

Our understanding of infectious disease has advanced from the naïve expectation that all pathogens evolve to cause less harm, to the realization that, although "it may be better to keep alive the goose that lays the golden eggs than to kill it... this argument depends on the assumption that, if you do not kill the golden goose, no one else will either" (Maynard Smith, 1989). This more realistic view of self-restraint in pathogens led to the conclusion that "competition between species or clones of one species within a host results in the evolution of greater virulence than would be favored with only one strain of pathogen" (Williams and Nesse, 1991). More recently, it has been recognized that cooperation among genetically related pathogens within a host may take the form of a collective attack on the host rather than restraint, in which case mixed infections may actually be less virulent (Brown, et al., 2002).

But what if unrelated pathogens actually attack each other? At Evolution 2008, Farrah Bashey-Visser (and coauthors Hadas Hawlena, Fabienne Vigneux, and Curtis Lively) presented data showing that insects infected by multiple strains of bacteria died less quickly, apparently because unrelated bacteria were killing each other using chemical warfare. Field sampling showed that many strains of these bacteria do indeed produce chemicals that kill other strains. They are, of course, resistant to their own toxic chemicals, because those that weren't left no descendants. So mixed infections do matter, but whether they are more or less harmful depends on the details of how pathogens interact within their hosts.

Mixed infectious also have important implications for beneficial interactions with hosts, a topic I emphasized in my own talk. For example, rhizobium bacteria inside root nodules on legume plants benefit collectively when some or all of them supply their plant with nitrogen, but this process is costly for the rhizobia. Free-riders would therefore undermine this cooperation, were it not for sanctions imposed by the host plant on root nodules (West, et al., 2002)(Kiers, et al., 2003). But rhizobia, too, are known to engage in chemical warfare, at least in the soil. I wonder what happens when two strains share the same nodule.

Durable cooperation

We generally assume that those paying the cost of mutually beneficial activities, such as nitrogen fixation, will be among the beneficiaries. But this may not always be true. Sam Brown spoke at Evolution 2008 on his work with coauthor Francois Taddei, on how "durable public goods" (those whose benefits may outlast those that paid for them) can affect cooperation. The collapsed bridge being replaced a short walk from the meeting site was paid for by gasoline taxes decades ago. (Today, we take the opposite approach, saddling future generations with debt to pay for current benefits, such as the war in Iraq. If you don't think this is a "current benefit", you must not work for Halliburton, Blackwater, or Al-Queda, rebuilding at a safe distance near the Afghanistan-Pakistan border. But I digress.) Similarly, bacteria produce and release expensive molecules that float around picking up essential nutrients, like iron. After the bacteria take the iron, they release the molecule back into the medium. Thus, the concentration of this "public good" depends on past, not just current production. Brown showed that, when public benefits come partly from past public benefactors, that can change the evolutionary stability of cooperation. For example, the frequency of cooperators and cheaters can oscillate, reaching a stable equilibrium much more slowly than if there were greater short-term dependence of public goods on the current frequency of cooperators. Brown and Taddei provide details in the open-access journal, PLoS One (Brown and Taddei, 2007).

More talk summaries next week...

Brown, S.P., Hochberg, M.E., Grenfell, B.T., 2002. Does multiple infection select for increased virulence? Trends in microbiology 10, 401-405.
Brown, S.P., Taddei, F., 2007. The durability of public goods changes the dynamics and nature of social dilemmas. PLoS One 2, 593.
Kiers, E.T., Rousseau, R.A., West, S.A., Denison, R.F., 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425, 78-81.
Maynard Smith, J., 1989. Generating novelty by symbiosis. Nature 341, 284-285.
West, S.A., Kiers, E.T., Simms, E.L., Denison, R.F., 2002. Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proceedings of the Royal Society of London B, Biological Sciences 269, 685-694.
Williams, G.W., Nesse, R.M., 1991. The dawn of Darwinian medicine. Quarterly Review of Biology 66, 1-22.

June 18, 2008

Guest blog: The Peacock's Tale

This week's post is by Dave Wisker, a graduate student in Molecular Ecology at the University of Central Missouri.

It's the creationist's dream. If actual evidence of creation is too much to hope for, how about a peer-reviewed paper in a respected journal overturning one of the icons supporting a major element of Darwin's theory?. Sexual selection in peafowl is definitely one of those icons. There appeared to be ample empirical evidence that peahen's preference for more elaborate trains on their mates has led to the spectacular male tail displays we see today. A series of papers in the 1990's by behavioral ecologist Marion Petrie and others seemed to solidly support this, and there is also evidence that elaborate tails may indicate good genes (Petrie et al, 1991; Petrie and Williams, 1993;.Loyau et al, 2005a). This, in itself, is a challenge to an older idea that the peacock's tail shows how arbitrary female preferences can be amplified to extremes by a "runaway"? process (Fisher, 1958). But, whatever their evolutionary origin, the preference itself has rarely been questioned.

However, a recent paper published in Animal Behaviour (http://tinyurl.com/4t69v5), "Peahens do not prefer males with more elaborate trains"?, challenges the conventional wisdom.

Mariko Takahashi and her colleagues studied a feral population of peafowl in Japan for seven years, and report finding "no evidence that peahens expressed any preference for peacocks with more elaborate trains (i.e., trains having more ocelli, a more symmetrical arrangement or a greater length), similar to other studies of galliforms showing that females disregard male plumage."? Intelligent Design and creationist groups have already praised this paper, saying it has demonstrated that the conventional evolutionary explanation for the peacock's tail is little more than a "just so"? story. A look at this paper and those from some representative studies that came to a different conclusion seems in order. Note: all of the studies looked at additional aspects of tail morphology besides eyespot number/symmetry, but this essay will focus only on this particular feature, for space reasons and because it is the heart of the 'controversy'. In addition, all of the biologists involved agree that tail ornamentation is only one of several display cues that a female uses in selecting a mate.

Takahashi's group noted that the number of eyespots, or ocelli, and their symmetry varies during an individual male's lifetime. So they photographed every male's train each season over the seven years, and devised a "Fluctuating Assymetry "index (FA) for each bird. The FA is defined as "a percentage of the number of eyespot pairs having lost one of the pair from a symmetrical linear position divided by the total number of eyespot pairs on the train."? The lower the FA value, the higher the symmetry, with a value of zero indicating perfect symmetry. They also used the number of eyespots as a different metric. Studies by Petrie & Halliday (1994) and Loyau et al (2005b), which did find that females prefer males with more elaborate trains, used eyespot number only. Petrie and Halliday removed 20 of the outermost eyespots from their treatment males using scissors (they did this without disturbing the length of the train), and used eyespot number as their metric. Loyau et al did not experimentally alter the eyespot number, but used the number of ocelli as their metric as well. So it appears all three studies used the same elaboration metric in at least part of their analysis.

Mating success was another metric. Petrie and Halliday used number of copulations for each male (after displaying and being accepted by a female), and the change in number of copulations for each male, if any, after eyespot removal. Loyau et al also recorded number of copulations after being accepted by a female. Takahashi et al took a different approach. They estimated male mating status "using female courtship behaviours. This was done to decrease the likelihood of excluding possible mates from the analyses because of limited observations."? Females show three categories of behavior when in a male territory: passing by the male, passively receiving his display, or actively soliciting a display by "run-around"? behavior. Takahashi's group noted that females who perform multiple "run-around"? behavior for a male often accept that male for copulation later, so they considered any female who performed more than two successive run-arounds for a male as having made a "preferred visit"?, and counted that as a successful copulation. This could be a crucial source of error, if a significant number of females performed multiple run-arounds but did not accept the male for copulation later, or if they copulated after less than three run-arounds. It's certainly worth investigating separately.

Takahashi et al point out that some of the studies which found a positive correlation between male mating success and train elaboration may be flawed because they only observed the birds in the morning, missing the crucial evening period of sexual activity. The creationists have especially harped on this. While it is true that Petrie and Halliday only observed in the morning, Loyau et al's paper specifically states they made observations from 0500 to 1700 hours. So that factor may not be significant in explaining the discordant results.

The Japanese authors also discuss other factors that may explain the different conclusions, namely sample size, length of study, and the age of the males involved. The advantage their study has over the others is the number of individuals (around twice that of the others), length of the study and the range of ages of the males. It is not clear, however, if those factors contributed significantly to the results.

Finally, this paper makes a very interesting observation: all of the studies of peafowl have shown very little natural variation in male train elaboration, regardless of the metric used. This suggests--to me at least--that one has to very careful in evaluating reproductive success, because the positive correlations were not particularly strong. If the males lack enough variation for females to make a choice, then it will be exceedingly difficult to discern female preference for elaborate trains in the wild. The fact that Petrie and others have added experimental variation and detected apparent selection gives one reason to think that, at this point, the evidence still suggests that females do prefer males with more elaborate trains. Suppose your hypothesis was that women prefer men with cars. If every man in your study group had a car, it would be hard to tell, from simple observation, whether female preferences were the cause of car ownership or not. You would need to take away some cars and see whether that has any effect. So the creationist's dream remains just that. However, these studies do inspire more research questions. How strong is the selection, if it exists? Is the low natural variation a direct result of female preference, that is, has the population reached its physiological limit for train elaboration? Does predation control the further runaway growth in train size/elaboration? What effect will this low natural variation have on the future of female preferential behavior? For example, Takahashi et al. found that a behavior known as "shivering"? be important. It looks like a fertile field for further investigation.


Fisher RA (1958). The Genetical Theory of Natural Selection, 2nd Revised ed. Dover. 291 pp.

Loyau A, M Saint Jalme, C Cagniant and G Sorci (2005a). Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus). Behav. Ecol. Sociobiol. 58: 552-557

Loyau A, M Saint Jalme, C Cagniant and G Sorci (2005b). Intra-and intersexual selectiojn for multiple traits in the peacock (Pavo cristatus). Ethology 111: 810-820

Petrie M, TR Halliday and C Saunders (1991). Peahens prefer peacocks with more elaborate trains. Anim. Behav. 44: 585-586

Petrie M and A Williams (1993). Peahens lay more eggs for peacocks with larger trains. Proc. R. Soc. Lond. B 251: 127-131.

Petrie M and TR Halliday (1994). Experimental and natural changes in the peacock's (Pavo cristatus) train can affect mating success. Behav. Ecol. Sociobiol. 35: 213-217

Takahashi M, H Aritat, M Hiraira-Hasegawa, and T Hasegawa (2008). Peahens do not prefer peacocks with more elaborate trains. Anim. Behav. 75: 1209-1219

June 13, 2008

There are none so blind...

A tiny little box labeled "correction" in the latest issue of Nature alerted me to a re-examination of data supposedly showing discrimination against female authors by manuscript reviewers. This claim, echoed in a Nature editorial (now retracted), was based on data showing that the fraction of papers with female first authors increased in one ecology journal when that journal started withholding the names of authors from reviewers, a procedure known as double-blind review. It turns out that other journals in the same field showed a statistically indistinguishable trend (more female authors over time), even though they still provide author names to reviewers. Thomas Webb and coauthors of this re-examination, published in Trends in Ecology and Evolution, note that a larger study published in American Economic Review reinforced their conclusions: double-blind review does not increase relative acceptance rates for papers with female authors.

These results seem to show that one possible form of bias against women is relatively rare, at least in the disciplines studied. Knowing that authors are female apparently has no effect in either direction.

It would be really interesting to see whether double-blind review would have any affect on success in getting grants. Differences in success rates for male versus female scientists could have many causes. For example, female scientists may be younger, on average, giving them shorter publication lists (but perhaps also fresher ideas?). Or there could be sex discrimination (in either direction) by reviewers. A statistically significant improvement in grant programs trying double-blind review, relative to control programs not adopting this approach, would provide evidence for such discrimination. Note that if such discrimination were found, reforms stronger than double-blind review might be needed, as some reviewers would still be able to identify the source of a proposal even if, for example, publication lists were reduced to numbers of papers in each journal.

In my own grant proposals, I usually reveal that my star Ph.D. student, Toby Kiers, was (and is) female, which isn't obvious from her name. Could that be why my two recent grant proposals were rejected? Maybe I should try my own double-blind experiment!

I wish more people would apply the same intellectual rigor to identifying road-blocks to the success of women and minorities in science that we do to our other scientific pursuits. The fact that there are more male than female full professors is certainly evidence of past differences in hiring or promotion (presumably some combination of discrimination and other factors), but if we want to know whether there is discrimination in hiring or promotion today, we need to look at hiring and promotion today. Is an associate professor with a given publication record less likely to be promoted if she is female? Do we put too much emphasis on publications? And so on.

I am reminded of Donald Campbell's 1969 paper, "Reforms as Experiments" (American Psychologist 24:409). Among the insights in this classic paper is the following. In response to some problem (crime, for example), politicians change laws, funding levels, etc. If the situation improves, they credit their "reforms." But crime rates etc. vary somewhat from year to year anyway. Now here's the key point: reforms are most likely to happen in a year when the problem is worse than average. Therefore, simple random variation is likely to result in some "improvement" the next year, even if the "reform" had no effect at all. So, as a minimum, you need to compare changes over years in states that did versus did not institute the "reform." If the editors of Nature had read this paper, substituting "journals" for "states", they might have been less likely to jump to conclusions.

June 11, 2008

Evolution 2008 in Minnesota

This year, the Evolution meetings are here in the Twin Cities. Evolution 2008 is a joint meeting of the American Society of Naturalists (not the nudist organization), the Society for the Study of Evolution, and the Society of Systematic Biologists.

A quick search of the program found no references to atheism* or child pornography, but there will be plenty of talks about sex. You could spend all Saturday morning listening to lectures on Plant Mating Systems and all afternoon learning about Sexual Selection. On Sunday morning, if you don't have other plans, there will be talks on the Evolution of Sex from 8-12, among other choices. You have to pay the registration fee that covers the cost of the meeting to attend these talks, but Olivia Judson (author of Dr Tatiana's Sex Advice to All Creation) will be giving a public lecture:

The Art of Seduction: Evolution, Sex, and the Public
4-5 PM on Sunday June 22
Ted Mann Concert Hall
My students and I will give talks in the Species Interactions and Life History Evolution sessions. I will discuss some of the talks at the meeting in a future post. Before then, I may be a bit sporadic, getting ready for the meeting. Also, both of our latest grant proposals were rejected by NSF -- depending on how you look at it, there are either too many good proposals or not enough money -- leaving us with essentially no funding for our research. So I'll be working on revised proposals due in early July.

*Note to those not in the US or Turkey: religious extremists claim that understanding evolution leads to atheism which then leads to crime. Comparisons among countries appear to support the evolution<=>atheism link but not the atheism=>crime link.

Explaining the evolutionary persistence of persisters

This week's paper is "Nongenetic individuality in the host-phage interaction"?, published in PLoS Biology by Silvan Pearl and others. This is one of many recent papers on bacterial "persisters" a topic we are also starting to explore in my own lab.

Update: In 2010, we published a paper (discussed here) showing that the bacterial symbionts of alfalfa can form a much greater percentage of persister-like cells than most bacteria. When a starving cell divides, the mother cell keeps most of the resources and then goes dormant. We see this as an example of microbial bet-hedging.

When a large population of bacteria (in an infected person, for example) is exposed to antibiotics, a few of the bacteria may survive. One explanation, which is often true, is that these survivors have genes that make them resistant to the antibiotic. For the purposes of this discussion, it doesn't matter whether they have mutated versions of genes also found in the susceptible bacteria, or an extra gene acquired by horizontal gene transfer from another bacterial cell. Either way, those without the gene (or with the nonmutated version) mostly get killed by the antibiotic. Therefore, subsequent bacterial generations are founded mainly by these surviving resistant mutants. Therefore, the frequency of the resistance gene increases over generations: a classic example of evolution.

Sometimes, however, testing the "evolved"? population for antibiotic resistance shows the same results as in the previous unevolved generation: most of the bacteria die, but a few survive. If there's no change in gene frequency over generations, then the population hasn't evolved. But then why did any of the bacteria survive?

In such cases, the antibiotic-resistant bacteria may have been in a dormant, persister state. They aren't genetically different, just (in effect) asleep. Bacteria in the persister state are resistant to many kinds of stress that would kill them if they were actively growing, including antibiotics for which they have no specific resistance mechanisms. Earlier, I discussed a paper by Andy Gardner and others pointing out that, in addition to surviving stress, "going persister" reduces resource consumption, thereby freeing resources for nearby cells. If the beneficiaries are close relatives, then natural selection may tend to favor genes that trigger persistence more often. On the other hand, cells in the persister state do not grow and reproduce, so there's an opportunity cost to being a persister. These are the aspects of persistence that my grad student, Will Ratcliff, is working on now.

But back to this week's paper. If bacterial persister cells are resistance to antibiotics, are they also resistant to infection by viruses? The authors compared a mutant that forms more persisters than usual with its rare-persister parental strain. The mutants were relatively resistant to being burst by a virus that infects bacteria.

To see more details of this interaction, they used time-lapse photography to track the fate of individual bacterial cells under a microscope. The bacteria were genetically modified so that they glowed when genes key to virus reproduction were active. Viral reproduction was suppressed as long as the bacteria stayed in the persister state, but once they started to grow the viruses could reproduce and burst the bacterial cells.

I've never been quite clear on why it's important to keep taking antibiotics for so long. I recognize that one could start to feel better well after only 95% of the bacteria have been killed, and the remaining 5% could quickly rebound. But why do some of the bacteria take much longer to die than others? There are probably various reasons, but the risks posed by persisters may be one of them. Every day, some fraction of persisters resumes growth, making them once again susceptible to antibiotics. (Or, in the case of this week's paper, susceptible to viruses.) The longer the treatment is continued, the more persisters will come out of hiding and die.

For more on the wonderful world of bacteria, see recent blogs by Carl Zimmer and Olivia Judson. Small Things Considered is usually interesting, too. And The Evilutionary Biologist is an expert on the viruses that attack bacteria.