Revisiting Hamilton and Zuk 1982

In a paper published in Science in 1982, William Hamilton and Marlene Zuk showed positive associations between the level of chronic blood infections and  display characteristics across North American Passerines. Based on these results they proposed a “good genes” model of sexual selection (Hamilton-Zuk Hypothesis): display characteristics used in mate selection are indicators of parasite or disease resistance. Twenty-four years after the paper was published, I spoke to Marlene Zuk about how this study came about, her collaboration with Bill Hamilton and what we have learnt since about the Hamilton-Zuk hypothesis.

Citation: Hamilton, W. D., & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites?. Science, 218(4570), 384-387.

Date of interview: 19th October 2016 (via Skype); 19th December 2019 (in-person at Centre for Ecological Sciences, Indian Institute of Science, Bangalore)


Hari Sridhar: I want to start by asking you a little about your motivation to do the work presented in this paper. I looked up your publication profile in Google scholar and it seems like this was the first paper you published.

Marlene Zuk: I was a graduate student at the University of Michigan and taking a seminar course with W. D. Hamilton, who was on the faculty there. And he was, and had been for some time, interested in the effect of parasites and pathogens on a whole range of things in host ecology, evolution and behaviour, and had already published, and was working, on the role of parasites in the evolution of sexual reproduction itself. Then, he was getting increasingly interested in whether parasites were also important drivers in sexual selection and mate choice and the evolution of secondary sexual characteristics, like the peacock’s tail. And for that he wanted to not just do modelling or theoretical work; he wanted to see if his idea would hold up in actual data. I was in the seminar and we were talking about it and he wanted to do a study looking at whether birds that had more ornaments were also more likely to be subject to parasites and pathogens. And I’ve been a birder for a long time and thought that sounded like an interesting idea. So we started working together on it. And then once we had the results, and they looked interesting and supportive of the hypothesis, we decided to make it into a paper. And yes, it was indeed my first academic publication, and it was a great experience working on it with him. I remember him asking whether we wanted to send it to Science or Nature, because he did feel like it was a an important contribution  – and I had absolutely no basis for judging whether it was or wasn’t, but was obviously going to go along with his ideas. I don’t know, maybe because I’m American, I said, Oh, I think we should send it to Science and so that’s what we did.


HS: Okay, that’s an interesting story. You said you did this when you had already joined graduate school. At that point did you already know what you were going to work on for your PhD?

MZ: No, not at all. I think it’s interesting to think about and I think about this a lot when I work with my own graduate students. Now it’s much more emphasized to have entering students know very concretely what they want to work on, sometimes to the point where they come in to work on a specific project, and I always have felt glad that Michigan didn’t do that. They did want you to identify a potential adviser; I came in thinking I wanted to work with Dick Alexander who also was, you know, a well-known figure in social evolution and animal behaviour, and didn’t really know much about Hamilton at the time that I started graduate school. I just discovered that I was really interested in the work that he was doing and so I ended up working with him. For a long time, I thought I wanted to work on birds, and then that didn’t quite pan out as I’ve ended up doing most, though not all, of my research on insects. I started graduate school in the fall of 1980. I think when I took the seminar, it would have been, probably, the winter semester of 1981. And then we did the work over the summer and fall, wrote it up , maybe over 81-82 and then paper came out in ’82.


HS: Did Hamilton eventually become your PhD supervisor?

MZ: Yes, he did.


HS: What was the seminar itself about?

MZ: You know I can’t remember what it was called. That’s an interesting question. I’m sure it was something had to do with social behaviour, evolution and cooperation. We also did some other reading. He was an interesting man in that he had a lot of diverse interests, and so if he had something that he was pursuing then he would just have people read something with that and we would discuss it.


HS: I notice that parasites and sexual selection in crickets has a life-long interest, which started with this paper and continued into the work you did on crickets for your PhD.  How did you choose to work on crickets?

MZ: I wanted to work on parasites and sexual selection. I toyed with working on birds for a while and I had a project in mind that I think still could be very successful,  but not as a PhD, which was to compare parasites and mate preferences in swallows.  Swallows are an interesting group because they’re cavity nesters, and so they tend to get a lot of parasites. But there’s “monomorphic bright”, “monomorphic dull” and “dimorphic bright” species just within swallows in North America. So you could look at purple martins, you could look at cliff swallows, and you could look at tree swallows. The problem is they all have the same breeding season, so you’d make yourself crazy trying to study them. I also spent a little bit of time trying to get ectoparasites off of swallows, based on this technique that I had heard about, where you stick the bird in a plastic bag that’s got an ether-soaked ball of cotton in the bottom and then wait for the parasites to fall off. And all that got me was a bird looking up at me like, “what are you doing?”; it didn’t really pan out. Hamilton worked on insects, and I always liked insects and I thought okay, this is going to be better to do on insects. I wanted an insect that had a sexually selected characteristic and that led me pretty quickly to singing insects. I spent my second summer in graduate school, going around collecting and looking at a bunch of different orthoptera, dissecting them, looking for parasites. And also Bill Hamilton arranged for me to go to a USDA lab in Bozeman, Montana that did insect pathology where I got kind of a two week crash course in how to look for parasites and insects, which was very useful. And then at the end of it all, I concluded that the field crickets n would be really suitable because they got a parasite that was sub-lethal that I could manipulate and so forth. And so that’s how I settled on that. I really didn’t start collecting data in earnest until the third field season, the third summer, after joining graduate school. Now I feel like people are much more pressured to start much earlier than that. And it was kind of nice because, you know, Bill didn’t really care and it was all time well spent.


HS: Stepping back a bit, could you tell us how you got interested in birds and in biology?

MZ: I’d liked insects for a long time when I was a child, partly because I grew up in a city. In a city, if you wanted to look at animals, insects were what you had to do, because it’s not like there were deer or elephants in my backyard. It took me a long time to realize that being interested in animals and being a biologist could be the same thing. I’m what we now call a first generation college student. In other words, neither of my parents had been beyond high school. I mean, they were perfectly supportive of my going to college, but they didn’t know anything about what one would do or how one would study different topics. And so, I think I probably assumed, as most students do who have any interest in science that I would be a doctor. And then I realized that one could actually study things like ecology and evolution and behaviour. And I started looking at birds when I took a class as an undergraduate that was on evolutionary ecology of terrestrial vertebrates.


HS: Which city did you grow up in?

MZ: Los Angeles.


HS: And where did you go to college?

MZ: My undergrad was at UC Santa Barbara, which was a wonderful place because it’s right on the coast. And there’s a lot of fantastic nature around there. There were a lot of classes you could take about insects and other arthropods and birds and mammals and reptiles and amphibians.  And you could go outside for a lot of that study. And plus, there was the ocean, and so there were marine invertebrates. I only now realize what an amazing place it was.


HS: In the US at that time, could you start a PhD immediately after an undergraduate degree?

MZ: You could, but I didn’t. I did a lot of different things first. I wasn’t at all sure what I wanted to do. I’m certainly not one of those people that knew I wanted to be a professor since forever. And I had a whole bunch of part time jobs. I did some technical writing, I worked in a vertebrate zoology museum, and learned how to prepare specimens. I taught a class for fifth and sixth graders, at a natural history museum. I also did a bunch of tutoring in math and chemistry for students who’d been admitted to the college but weren’t necessarily all that prepared for quantitative classes. So, lots of different things.


HS: Was all this in Santa Barbara?

MZ: Yes, I stayed in Santa Barbara after I finished my undergraduate.


HS: When did you start thinking about doing a PhD?

MZ: You have to apply the year before. I really liked the job I had toward the end, which was this tutoring position. But it was clear that that kind of job was going to be harder to maintain, because the political situation was such that they weren’t necessarily offering a lot of programming to support students like that.


HS: What was it like then to apply for a PhD program? How did you choose to go to Michigan?

MZ: I don’t think it’s really changed that much. I asked my former professors, you know, “So I’m interested in animal behaviour” –  I don’t even know if I said particularly in sexual selection; I might have –“where would you recommend that I go?”. And they suggested several different places that they thought had good departments. The one difference is that instead of going online to read papers by people, I had to go to the actual physical library and look through actual physical journals to read their papers. But otherwise, it’s not that different. And then, you wrote to people, and again, instead of emailing them, you had to write to them. But then you wrote to them, and they answered.


HS: You mentioned earlier that, initially, you wanted to work with Richard Alexander..

MZ: Originally, I was going to, because I had read some of his papers and really liked them.


HS: Can you tell us a little more about how you and Hamilton actually worked together on this project? How did you find the time to do this, did you sit together and look at the data together etc.? Could you give us a sense of how this collaboration actually worked?

MZ: He had already realized that, just by happenstance, the literature contained – well, and still does- a lot of datasets where people went out and caught birds in mist nets, put identification bands on them and released them. And when they did that, they would often take a drop of blood, make a smear of it and look for blood parasites in the sample. That was going to be a much better source of information about parasites that could then be linked to brightness than trying to find other experimental work that people have done. I can remember sitting there and going through – of course, again, at that time you couldn’t do anything online -these big back-issues of journals in parasitology and deciding which data sets are going to have a more complete set of birds that I’m gonna be able to rank. We decided early on that I would go through the list of birds – the host species – and rank them in terms of brightness before knowing anything about their parasite prevalence from the papers.  So I would just make species lists, and later on we’d add in how heavily parasitized they were. And then we both worked together on the analysis. I can remember sitting in a class and writing what eventually became the first few paragraphs of the paper itself. It was a lot of fun because, you know, most people would say, why would there be any connection between how many parasites a bird has and how brightly coloured it is. And to be honest, for a while, I was slightly puzzled by it too, when I first started working on it. As a new graduate student, you’re desperate that no one finds out how ignorant you are about pretty much everything. I can remember thinking: this doesn’t make sense to me because … see, the kinds of parasites you expect to drive cycles in the evolution of sex itself are different than the kinds of parasites you expect to drive sexual selection. And I had been used to thinking about the models that Bill was talking about, having to do with the evolution of sex itself. Why are we looking at these blood parasites, because they have really different life cycles? So, in a sense, I really did do it blind because I was puzzled, at least until we started working on the analysis after I’d done the rankings. I was kind of puzzled about why we were making this connection even, myself, and then eventually figured it out.


HS: How difficult was it to locate papers that had relevant data?

MZ: Oh, it was really easy to find them. At that time, for whatever reason, there was kind of an explosion of people who would go to a national park, or they’d go to some area that was on a migratory flyway, and they’d net birds and put, you know, rings or bands on them. And when they did that, they’d take a drop of blood, make a smear, and someone later would look for parasites. And so all you needed to do was use those data sets, and then put that together with ranking the birds for brightness.


HS: On this trip to Bangalore, you have conducted a workshop on the challenges that women face in doing science. What was it like, at the time when you were doing your PhD?

MZ: I think it was more difficult, partly because there were far fewer women faculty members, and also because there was a lot of behaviour that was tolerated, both in terms of sexual harassment and gender harassment, that I think now people would today recognize as being completely out of line. At that time, everybody just shrugged and said, “Oh, that’s how these people are like” and, you know, you just got on with it. I think there were some difficult things about it. Certainly, there were people I knew who dropped out of science, or dropped out of a program, because of those issues. My cohort at Michigan started out with nine people of which three were women. I was the only woman that finished.


HS: Earlier, you said a little about the writing of this paper; do you remember approximately how long it took you to write this paper up?

MZ: No. And it’s funny because I’ve also written several books and have done, well, obviously lots of other writing with various scientific papers, and I always find the question – how long does writing take – to be a really difficult one to answer because you’re never just saying, Oh, okay; from 8 to 5 today, I’m writing. It always gets done in bits and pieces. So, I’ve always found that question pretty much impossible to answer.


HS: You said that you might have been able to say which parts of it you wrote and which parts Hamilton wrote. Could you still do that?

MZ: It’s funny, I’ve known that you were going to talk to me for ages, and I’d actually meant to bring up a version of the paper, because it’s not like I read it every day. But I remember I actually wrote out the explanation about how frequency dependence works, I wrote the part that’s got, you know, imagine that there’s a host and a parasite with two alleles; I wrote that part. I remember he wrote the part about thinking of sexual selection as if the female is a physician doing a physical examination of the patient.


HS: You mention a person by the name of M. Perrone, who ranked the songs of the birds blind. Can you tell us a little more about who this person was? Was he or she also a student in the university?

MZ: Oh no, he was actually a guy I was dating at the time, who was an absolutely avid birder. And so we thought he would be a good person to go through and think about the songs, because he had heard and was familiar with pretty much all the birds of North America.


HS: If you don’t mind, can we also go over the other names in the acknowledgments, just to get a sense of how they helped?

MZ: Ok.


HS: Wallace Dominey

MZ: Wallace Dominey was a post-doc in the department at the time, who worked on fish mating systems and sexual behaviour. And he attended at least some of the seminars, and was interested in the topic. So, he would have been someone with whom we would have discussed the idea.


HS: Ilan Eshel

MZ: Ilan Eshel is a really good mathematician and theoretical biologist with whom Bill had worked on the evolution of sexual reproduction, and on some of the models having to do with limit cycles in maintaining sex in the face of parasites.


HS: Paul Ewald

MZ: Paul Ewald was also a post-doc at the time, and is now a professor at the University of Louisville. He has been one of the champions of evolutionary medicine writ large, and of trying to understand how parasites and pathogens evolve in concert with their hosts. He’s written a couple of really cool books, one called  Evolution of Infectious Disease. He worked a lot on the how vector-transmitted diseases are expected to evolve to very different levels of virulence than directly transmitted diseases. He was one of the pioneers in a lot of those ideas.


HS: Peter Grant

MZ: Peter Grant of course is the famous Darwin’s finch evolution person, among other things.  He was also on my committee and a professor at the University of Michigan at the time. He and Bill were close colleagues and friends.


HS: Lester Lee

Lester Lee was a graduate student who, again, was in the seminar, and tragically died quite a number of years ago. He was also interested in evolutionary biology.


HS: Trevor Price

MZ: Trevor Price is now a distinguished biologist at the University of Chicago and works – well, he worked on the Darwin’s finches for his PhD with Peter – and then went on to do a lot of really important work on speciation and ecology in Himalayan warblers. So he actually spends a lot of time in India.


HS: Richard Wrangham

MZ: Richard Wrangham, who is now at Harvard, is an anthropologist and a primatologist, who was at Michigan at the time and was a colleague of Bill’s, who was also interested in the ideas.


HS: Were all these people at Michigan?

MZ: Well, Ilan Eshel was not at Michigan, but he was certainly a close colleague of Bill’s, and so he talked to him about a lot of stuff.  But everybody else, you know, like all the discussion people, were at Michigan.  Richard Wrangham was at Michigan then and so was as Peter Grant and so was Paul Ewald and so was Trevor Price.


HS: I notice that you don’t mention any funding for this study.

MZ: We didn’t need any funding. I mean, it was just all done from books. And, I was already TA-ing, so I had support from that.


HS: Do you remember how you decided the authorship order?

MZ: It’s funny because, I think, only in the last maybe 15 years, maybe less than that, has this changed. So it used to be that in molecular biology, the last author was the person whose lab it was in, and so their name went on everything. But in ecology and evolution, no! In ecology and evolution, the first author was the person who was really responsible for the work. And then after that, it was the second author who had done the second most contributions, the third the third most and so on and so forth. And it’s only very recently  – well, I’m not sure whether you think 10 years is recent or not –  it’s only within about the last 10 years or so that that’s changed. Now last author is viewed as an influential authorship in ecology and evolution, as well as in molecular biology. It really was Bill’s idea. And you know, we didn’t really talk about it.


HS: You said that Science was the first place you submitted this to. Do you remember if this had a relatively smooth ride through peer review?

MZ: I had nothing to compare it with. And Bill, of course, was the corresponding author, so I don’t remember terribly clearly. I do remember meeting someone at a conference, quite some time afterwards, who said that they had gotten the paper to review. And now I honestly can’t remember her name, but she said that it had just sort of arrived and she was excited by the paper. I certainly don’t remember there being a lot of backing and forthing with it. It is partly because, you know, now, I would kind of know what to expect, but at the time, I just didn’t know how that stuff worked.


HS: At the time when the paper came out, do you remember if it attracted a lot of attention, both within academia and in the popular press?

MZ: Yeah, a little bit in the popular press.  I ended up writing an article for Natural History magazine summarizing our work, to the extent that you can call that popular press. The reaction among scientists was, I think, two-fold. Traditional parasitologists and people who had  been studying disease in animals, in wild animals, pretty much hated it because they thought, first of all, that we were just coming up with a completely improbable suggestion about the effect of parasites on their hosts. Whereas, I think, more traditional evolutionary biologist probably was more inclined to give it some credence, because of who Bill was. So, you know, it’s a fair question that, had it been me and someone that no one had heard of, whether we would have gotten very far with the idea. Obviously, I can never answer that question, but I think it’s a fair point that potentially not.


HS: Did you anticipate at all that it would become such an important contribution to this area of research?

MZ: Oh god no!


HS: It’s been cited over 3000 times and it gets mentioned in all the text books. Do you have a sense of why it is attracted so much attention, and what does it get cited for mostly?

MZ: I actually think that, in part, we were lucky, in that it was part of an idea whose time had come, from several different parts of biology. People in evolutionary ecology were starting to realize that, Oh, we’ve been neglecting the effect of parasites and disease for quite some time. So Peter Price for instance wrote a great book on evolutionary biology of parasites, which, I think, was published in 1980, which really paved the way, I think, in a lot of respects. Anderson and May published a couple of papers, in 1979 I think, on the role of parasites in population regulation, which, I think, were highly influential. Plus I think the methodology was just getting easier. Charles Elton, in his ground-breaking ecological stuff from the early part of the twentieth century talked about the role of parasites in regulating host populations. But how can you tell? It’s even harder to study parasitism than it is predation and you know even with predation you don’t observe it very often. So I think there had long been this idea that, yeah, this is probably a big deal, but we don’t know how to study it. And then as it became easier to, both, do samples of wild animals, it became easier to do the laboratory work necessary for identifying parasites, and it became easier to do the kind of comparative analysis that we attempted. So I think it’s not that no one had really thought about it before, but it wasn’t clear how to apply it.


AK: This paper came early in your PhD. Did it have any kind of impact in terms of where you went next? That’s the first part of my question. And the second is, how did do you think it influenced the future trajectory of your research? Did it lead to new things you wanted to try out?

MZ: I’ll answer the second part first, which is that, although, a lot of my research has not been directly testing the hypothesis in that paper, I became convinced very early on that parasites and pathogens were important. I did work more directly on the effect of parasites on sexual selection in junglefowl, which is what I did for my postdoctoral research. And a lot of my PhD research, which was on parasites in crickets, also had to do with that. And now I work on a parasitoid, again in crickets.


HS: Today, it’s 34 years since this paper was published. Would you say that the main conclusions from this paper hold true still, more or less?

MK: Sure, more or less, although it’s also really clear that parasites alone are not going … and we actually recognized this then too, that parasites alone are not ever going to explain all the variation you see in secondary sexual characteristics among species. The other major thing that’s happened since we did that work is a growing recognition that it’s not parasites per se, it’s the immune response and resistance to those pathogens, which are going to play a role in the evolution of secondary sexual characteristics. And I think that there’s been a lot of really interesting work on what’s now called eco-immunology.


HS: If you were to sort of redo this study today, or if you have already done a similar study, in what ways would it be different. Would you change anything about the way you did the study, given the availability of more data or  the theoretical development since then?

MZ: The main thing would be that now the methodology for doing computer analyses in general and comparative work in particular is so much more sophisticated than it was.


HS: Have you or has anyone else done a similar sort of analysis later on.

MZ: There have been a number of attempts, both in birds and in some other taxa, you know, people tried doing similar sorts of things in different ways. There have also been a couple of meta-analyses looking at different within-species tests as well as among-species tests, and you know so forth. So yeah, I think there have been quite a few.


HS: I want to ask you about certain specific sections off the manuscript where you hinted at things that were unknown then and that might be future directions for research. One of the things you say is, “The positive association found for female brightness might follow from imperfect sex limitation of gene expressions only selected for in males. However, we prefer the idea that in monogamous birds, sexual selection aiming at genes for health can be working in both sexes at once”. After that paper, has there been more work on female brightness itself and how that is linked to parasites.

MZ: Oh yeah, and certainly on the idea that there’s mutual mate choice in monogamous species. So the answer is, yes, there have been both on the idea of whether there’s simply female brightness being dragged along by selection on males or whether there’s mutual mate choice. There’s certainly a lot of work done on that. Trevor Price has, in fact, done some work related to that which is extremely interesting. But one big thing that’s changed since then, that we didn’t know about the time, is the discovery that in, so called, socially monogamous birds there’s actually a lot of extra pair paternity. That kind of throws a monkey wrench in the whole thing because, what previously seemed like monogamous species, now is looking more like non-monogamous species, at least genetically. So I think that’s been a huge change that’s happened since that time.


HS: In one of the notes to your paper you say that the evidence for the relationship between parasites and secondary sexual traits within species was very scanty and equivocal. I wanted to ask you whether, since then, you have worked on this aspect and whether there has that been work on this from others too?

MK: I think a lot of people started doing that after our paper was published. That’s what a lot of what my post-doc was about, looking at exactly those questions in red junglefowl.


HS: Towards the end of your paper you say “Evaluation of the many plausible and overlapping theories proposed about display and sexual selection, including our new one, is a daunting task and must be left to the future”. To what extent has that happened?

MK: Everybody always says more research is needed. How can you not say more research is needed! So, I don’t really think there’s anything particularly profound in that. I do think that at the time people were still not entirely convinced that, for example, female choice could be a sufficiently strong selective force to have produced some of the elaborate male secondary sexual characteristics that you saw. Now I think that’s been amply demonstrated. So certainly we’ve cemented that connection really well but that’s not to say that there’s not more work to be done. Now, for instance, what a lot of people are interested in is, now that we can probe the genome more closely, people are interested in finding out to what extent genetic interactions or genetic incompatibility or genomic conflicts between the sexes are responsible for the patterns that we see. That’s an area that was just unknown to us at the time.


HS: Have you ever read the paper after it was published?

MZ: I don’t know, probably, because there was some re-examination of it several years later So, yeah, I probably did.


HS: If you compare this paper to the papers you write today do you notice any striking differences?

MZ: Oren Harman, a historian of science who visited  our university awhile ago, said that there shouldn’t be this distinction between writing that you do for an academic audience and writing that you do for the public. The only distinction is there’s writing that makes you want to turn the page and there’s writing that doesn’t. I thought that was actually rather nice.


HS: Would you count this as one of your favourites among all the papers you published?

MZ:  Sure. That’s not difficult. I probably have a lot of favourites, but yeah, absolutely, this is one of my favourites.


HS: Could you tell us a little more about why what it is you like about this paper?

MZ: I think it’s got an absolutely original idea, which I thought was super fun to get out there. I met, who was it, Don Strong, who came to visit when I was a faculty member at UC Riverside. He had heard of me because of that paper and he said, Oh yeah, I remember when that came out, and it was interesting. I don’t know if it’s right but then most people don’t even get to be wrong! I think it’s not an original saying to him, but I think it is a nice way to think of it, that might not be right, but most people don’t even get far enough for people to think they’re wrong.


HS: What would you say to a student who is about to read this paper today? Would you add any caveats to his or her reading?

MZ: No. On the one hand, of course you should always read things with the eye towards what else was going on in the field at the time. And so you know one could talk about that. At the same time, I think papers should stand on their own; otherwise, everything becomes impossible to understand unless you have all this other information. I think it should be read on its own terms.


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