Revisiting Kokko et al. 2002

In a paper published in Proceedings of the Royal Society of London London B, Hanna Kokko, Robert Brooks, John McNamara and Alasdair Houston integrated ‘Fisherian’ and ‘good genes’ ideas into a general model of female mate choice for indirect benefits. Fourteen years after the paper was published I asked Hanna Kokko how she got interested in this topic, her memories of carrying out this work, and what we have learnt since about female mate choice for indirect benefits.

Citation: Kokko, H., Brooks, R., McNamara, J. M., & Houston, A. I. (2002). The sexual selection continuum. Proceedings of the Royal Society of London. Series B: Biological Sciences, 269(1498), 1331-1340.

Date of interview: 5th December 2016 (via Skype)


Hari Sridhar: I would like to start by asking you what your motivation was to do the work presented in this paper.

Hanna Kokko: So it actually starts from an earlier paper that was published in Ecology Letters. And that, in turn starts with an encounter with Rob Brooks, who is the second author of this 2002 paper . I think it was the year 2000 when there was the ISBE International Society for Behavioral Ecology conference in Zurich – the city where I live now; that’s just a coincidence – and that’s where I first met Rob Brooks, who then was giving a talk about his very fancy result on guppies, where basically he was saying that his results favor the ‘Fisherian’ rather than the ‘good genes’ process, when it comes to explaining why females are preferring this trait. I had never met him before, but I remember sitting in the audience and thinking, hey, but hang on.  If I just explain a little bit what’s going on there – it seemed like, by mating with these more attractive males, the females were getting more attractive sons, but not at all better surviving sons or better performing daughters in any sense.

But then, I think it was during that talk that an idea came to me, kind of like an alternative explanation that, maybe the better males are actually intrinsically better, but they can get so much benefit out of putting that all allocation-wise into attractiveness, rather than into survival traits, assuming that there’s a trade off. He hasn’t actually shown that it’s this process as opposed to that other process. And of course, when you’re a young scientist – I was much younger then – you’re kind of nervous about criticizing somebody, so I didn’t dare to do that during the conference. I thought that I need to write up my thoughts. And then I wrote it up as a manuscript format and sent it to him. I can’t remember if it was before or after publication; I think maybe before. And I totally expected that, you know, this person might hate me and that kind of thing. But he responded incredibly positively saying that this is fantastic and interesting, and why don’t you, … I think I had a plan of visiting Australia back then anyway. So, he was actually the first person I met on my first ever Australia visit. That critique I wrote became an Ecology Letters paper; Rob brooks is not on that paper. But we started talking about a much more general way to formulate this, to not just kind of empirically make a point that, well, we don’t really know what’s going on, but doesn’t this mean that the whole dichotomy is a bit of a pointless one, when, in reality, things always allocate this way or that way.  So, that’s how this paper then came about.


HS: Did you meet Rob Brooks for the first time at that meeting?

HK: I briefly met him during the ISBE meeting, but we didn’t really talk in depth about this one yet. It was later in Australia, where I went, I think, in 2001 for the first time, when we started talking about this and developing this.


HS: How did the other two authors get involved?

HK: Again, there’s another paper with them, which is kind of peripheral to the current one that we’re discussing. There’s a…boy I should check it, I think it’s 2003…paper about the mathematical ways to formulate these situations with tradeoffs, when there are two different sexes doing things. So, basically, the problem is that if you try to do something like a game theory approach or optimization approach, but you also know that genes flow via males and genes flow via females, it’s not really obvious how you should do this. John McNamara and Alasdair Houston were people who, back then at the time, were working on trying to understand how to do this. That’s how they became part of this. We never worked together in the same room. But because of this different expertise, they came on to this via emails and stuff.


HS: So you were already working on the paper that was eventually published in 2003?

HK: Yes. So, I mean, if you challenge me to remember in which order I was working on which paper I can’t tell you now. All the emails are on older computers and so on. But I was working on these; they were all working on these ideas at that time, sort of in the region 2002-2003.


HS: And you never met together as a group?

HK: Not as a group. I mean, I have met them. We have probably also been all together at the same conference. You know, john and Alasdair work in Britain and Rob works in Australia, so there’s quite a sort of big geographic distance. At meetings of course you can come together. But for this particular project, it was a lot of emailing.


HS: Can you tell us a little more about how this work happened? Did you do most of the work when you were still in Glasgow?

HK: Yes. I was working on modeling this in 2001. I think I went to Australia twice. I can check my notes if you want to have this totally exactly. But I spent a couple of months every time there, and I was based in Canberra, rather than in Sydney where Rob is, but we met several times.


HS: Do you remember, roughly, how long it took you to do this, the modeling work itself and writing up a draft of the paper?

HK: I mean, I was working on other things simultaneously. I can only guess maybe half a year.


HS: Can we go over the people you acknowledge to get a sense of how you knew them and how they helped?

HK: Yeah sure, I have the paper in front of me.


HS: M. Jennions

HK: Michael Jennions I met in 2001, which was my first visit to Australia. And we formed a collaboration that has carried on until the present day. I think the last time I sent him an email was this morning! And he was very interested in this project from the start, and became an author on a 2003 review, which is kind of like talking about this model, and then also talking about how to model sexual selection in general, which I think is actually a better-cited paper than the current one we’re discussing. If I’d known him a little bit earlier, he might have well ended up an author here as well; he was very interested in this. Janne Kotiaho is a professor in Jyväskylä in central Finland. He, back then, was working a lot on sexual selection and had been interested in mortality effects of male traits. So, he was an obvious one to show the manuscript to, and he gave some comments. Ben Sheldon is an ornithology professor in Oxford. I can’t remember what his status was at the time, but we must have clearly felt that, you know, he would give insightful comments from the empiricist’s perspective.


HS: M. Blows

HK: Mark Blows. Well, there’s a list of names after that, who are all people who are interested in sexual selection. They are all therefore people who, you know, during this, whatever it may have been, half a year or something like that, we chatted with about these ideas. So, like when you thank somebody for discussions, right, it’s about kind of getting feedback, informal feedback, that way.


HS: I just noticed a reference to an unpublished manuscript, whose authors are McNamara, Houston, dos Santos, Kokko and Brooks. I’m guessing that was the 2003 paper?

HK: Yeah, that’s right. So I’m actually talking about two different 2003 papers. There’s the review. And then there’s this one, which was unpublished then, which is the other 2003 paper.


HS: Would you say that this paper had a relatively easy ride through peer review? Was Proceedings of the Royal Society the first place you submitted this to?

HK: I don’t know if it surprises you, I cannot remember. I think we may have initially submitted it somewhere else. Some people keep very good records of what happens with their papers, like, you know which journals they go through. If I had all my emails from…this is 15 years ago, I could check those kinds of things. But if I say something, you know, my memory really is unreliable about it.


HS: This, again, might not be something you recollect very well – At the time when the paper came out, you know, do you remember how it was received? Was it something that attracted a lot of attention?

HK: Yeah, it did. I remember there was a feeling that a lot of people talked about it, a lot of people chatted about it, there were certainly those people who kind of didn’t want to think about things this way. And then there were people who did want to think about this way. I think the argument for not adopting this kind of position is that, because it’s possible to build a model where one of the processes is not operating, therefore, they are kind of like, it’s useful to think of them as fundamentally different. To which I would say that, well yes, it is always possible to ignore, for example, kin selection from dispersal models, but in reality, kin selection is kind of like, it’s very hard to completely exclude it,  So therefore, you know, it may be healthiest to accept that, you know, these things are very intertwined in reality. So I’m quite relaxed about this, you know; I think it certainly made people think and that’s the point of science.


HS: In the Discussion of the paper you sort of anticipate this – you have e a list of counter arguments that might be raised to the model you’re proposing. I was curious about whether, you know, these counter arguments were in fact raised when the paper was published, or did you sort of preempt this with your list?

HK: Pre-empting is probably a good word here, because precisely those points, they would be pointless to raise when we have already talked about it. It was more like what I just said – this was a general feeling that it’s useful to think of the extremes as, kind of like, conceptually fundamentally very different things. That was, kind of like, the sentiment that was there. I also remember somebody wrote somewhere that, you know, this is such a complex model, it has, whatever, 17 parameters, and, therefore, isn’t it a bit of a special case. Of course, I feel that we included so many things just to show the flexibility, and that we need to think about quite a lot of things when thinking about real sexual selection instead of a very abstract one where some processes are excluded.


HS: This paper has been cited over 300 times. Do you have a sense of whether it is cited appropriately?  Do people understand the model?

HK: I just checked in Web of Science and found it is cited almost 450 times; so it’s quite a lot. I mean, you have to be realistic about how people cite papers. They don’t all, you know, go through all the modeling details and things like that, so often it’s just kind of like a relatively general comment; and that’s fine. If there’s something I sort of wish people would do a bit more is to really take Figure 4 as a sort of stronger take-home message. How, exactly the same process, depending on some sort of environmental conditions with, for example, a predator being present or not, can really shift the balance to look a bit more ‘Fisherian’ or look a bit more like ‘good genes. I sometimes think that, you know, if I was writing about this now, I would maybe emphasize that point a bit more. But, you know, I’m pretty happy about the impact that it’s made.


HS: Today, almost 15 years after the paper was published, is your thinking on this model similar to what it was 15 years ago, or do you think differently about this in any way?

HK: Yeah, I think what has happened in the last 15 years is that people talk quite a lot about genetic architecture of sexual traits – this is not a very genetic model at all – and the, kind of like, sexual conflict that can come about from these situations. So maybe, these days, if I was working on this, if I got this idea now, I might phrase it a bit more genetically. I might also phrase it a bit more in the, kind of like, conflict between males and females kind of angle. But I don’t have any major regrets. It’s just, kind of like, every paper, a bit of a product of their time.


HS: Does this continue to be an important area of research for you?

HK: No, actually, I don’t do a lot of mate choice these days. It’s not because of being bored of it or whatever. I think it’s just natural that your own interest flows in a direction that is not completely unrelated, but it’ll be boring to always, always, always work on the same thing. I’m very much interested in the demographic consequences of sex and sexual reproduction, and male-female differences. But mate choice per se is not my main major theme at the very moment. But I never completely abandon topics. It’s just, kind of like, if a cool idea arises at some point, then it might sort of come back into the forefront. But right now, it’s not the main thing.


HS: Immediately after this paper – I’m guessing this was sort of like a second post-doc – you went on to Finland. Did this become an important area of research for you then?

HK: Yes, so I did carry on that kind of thing. For example, the 2003 review, I think, it’s my best cited paper ever. Well, reviews often are, so that’s, kind of like, not so terribly surprising. But certainly I was continuing…I mean, it was important for me because it kick started this collaboration with the Australian people  – Rob Brooks and Michael Jennions  – and I have to varying degrees worked with them ever since.


HS: Did this paper have any kind of direct impact on your career itself? Did it come up or was it noticed when you were applying for jobs immediately after?

HK: Sure. I mean, it’s very hard to kind of disentangle the effect of one paper when, you know, there were others.  It was certainly something that showed that I’m able to do, kind of like, conceptually important work, but there are others from the time that I’m also quite proud of. I mean, it certainly hasn’t harmed.


HS: This is just a matter of detail, but I noticed where you start describing the model initially, you say, for the two alternative alleles i = 0 and 2. But later you say 1 and 2. Was this just a typo?

HK: Yeah, that probably is a typo. It should be 1 or 2. I’ve never noticed that.


HS: At the end of the paper, there’s a line where it says “As this paper exceeds the maximum length normally permitted, the authors have agreed to contribute to production costs”. Was this normal practice then?

HK: I think it still is. So it’s, kind of like, they try to keep the length short to encourage concise writing. But then they also accept that, you know, sometimes you just need to write a bit more because of whatever complication. Then, this is kind of like their way of having a little bit of financial punishment if you have to do that. Or, let’s call it  – encouragement to keep it short.


HS: In one place in the discussion you say, “an understanding of the underlying genetics will determine how easily additive variation is maintained”.  Do we understand the genetics better now?

HK: Oh, absolutely. I mean, if there’s anything that has been happening in this field, that is really different from back then, is, you know, the whole genomics becoming affordable, and people being able to figure out these kind of things much more than before. That’s certainly something that has become an active research field.


HS: On the same page you make some suggestions about what you think are the most important things to test empirically. You say, “the most important prediction to test is that females prefer males with high breeding values for total fitness”. Then you also say “Nevertheless, it remains worthwhile for empiricists to ask whether females seeking indirect benefits usually gain value by producing sexy sons or if offspring survival fecundity is also improved”. And then, towards the end of the paragraph, you say “a testable prediction from our model is that the tradeoff between mating success and other components of fitness will co-vary with the cost of mating”. Have these predictions been tested empirically, either by your group or by others?

HK: Well, this gets quite philosophical because, some of these results or predictions, they are about saying that we should measure something that’s very, very tiny. So, for example, this very cheap female choice – we can intuitively say that, if a female just sort of has to have one look at 10 different males and make a decision, that’s probably very cheap because it’s kind of like, you know, her eyes are open anyway, whereas some sort of expensive mate sampling, having to have sort of big travel distances and things like that, is probably more costly. But actually putting a number on those costs in an ecologically relevant scenario, is just really, really hard. And maybe back then, you know, maybe one was a bit optimistic that at least people would, sort of, put some sort of rough axis values on that. I don’t know of a paper that has explicitly tested that across species. On the other hand, you know, I haven’t checked all the 400 citations that this has gotten, but I think I would know if such a thing existed.


HS: Immediately after that, another thing  you highlight is that “it also remains valid to ask whether indirect benefits differ between offspring sexes”. Is that something that we know more about now?

HK: Yeah, that’s probably something that we do know much more about. So the entire field of sex-specific fitness effects and sexually antagonistic traits, that’s a very active research field right now.  Certainly, there’s more there, better than with the previous paragraph.


HS: And is this something you’ve worked on yourself?

HK: Well, I’m not an empiricist, so I have not contributed directly to knowing more about that. On the other hand, I still work on the sort of conceptual clarification of these kinds of things. So, for example,I have a book chapter from two years ago, I think, about the relationship between sexual conflict and sexual selection in mate choice. It’s one of those Cold Spring Harbor press things,  trying to sort of link those two fields together in, hopefully, a nice way.


HS: Have you ever read this paper after it was published, and if you have in what context?  

HK: Well, mostly I think because I have, over the years, mostly with Michael Jennions, produced quite a number of book chapter style reviews on this topic. And then you often end up citing your own work, and then you want to check what you actually said, because one’s thoughts evolve and one sort of starts having ideas about what you probably already wrote in the paper, but it’s actually an idea that you only got later, so therefore you need sometimes to go back and read what you were thinking at the time.


HS: Would you count this as one of your favorite pieces of work, among all the work you have done?

HK: Yes, I would say so. I think it was motivating, not only because it was intellectually quite exciting, but also because it was such a wonderful experience of working together with somebody where the collaboration actually started when I was thinking, Oh, dear, I need to criticize this person, and that he took it so wonderfully. I think it’s just a great example of the way science should work, when people are open-minded and generous and all that. So that sort of creates a positive feeling as well.


HS: What would you say to a student who is about to read this paper today? Would you point them to other papers they should read along with this? Would you add any caveats?

HK: I think it’s quite a self-contained piece. Maybe it will be good to read it together with the 2003 review. And then, of course, you know, nowadays there are much later and kind of like more up-to-date reviews of work that obviously couldn’t exist back then. But I still think that people tend to think that it makes a point that can be understood, by reading it just like that.



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