Category Archives: Evolution

Science journalism blows it, dolphin rape edition.

A few weeks ago I got into a discussion on Twitter with Ananyo Bhattacharya, online editor of Nature News and writer for The Guardian’s science section, after he put out a call asking for ways to improve science journalism. During that conversation, I argued that one way to do this is to create a culture of journalism that values scientific knowledge and expertise as a core value[1]. Ananyo seemed unimpressed with my viewpoint, and suggested that the main point of science journalism was to pry into the dark corners and root out biases, fraud, and the like in science. He views scientific communication and scientific journalism as two distinct things (and thinks that journalists doing ‘PR for science’ is ‘drippy’). Indeed, when asked directly during a Royal Institute forum on science journalism whether journalists should read the original papers behind the stories that they write, he dismissed the idea:

“If the question is ‘must a good science journalist read the paper in order to be able to write a great article about the work’ then the answer is as I said on Tuesday ‘No’. There are too many good science journalists who started off in the humanities (Mark Henderson) – and some who don’t have any degrees at all (Tim Radford). So reading an academic research paper cannot be a prerequisite to writing a good, accurate story … So I stick to the answer I gave to that question on the night – no, it’s not necessary to read the paper to write a great story on it (and I’ll also keep the caveat I added – it’s desirable to have read it if possible).”

He further suggests, in the same comment (original source), that if journalists had to read original papers than no one could report on particle physics[2].

I’m not going to try and hide my bias here: I don’t like Ananyo’s viewpoint on this. I don’t think that it will lead to good writing, either of the communication or journalistic variety, but more importantly I think that forcing journalists to read the papers before they write an article might have stopped stupid @#$@ like what happened today from happening at all.

The story: I received an e-mail this morning from Dr. Bill Sherwin, a member of the Evolution and Ecology Research Centre (E&ERC) here at my current institution, the University of New South Wales. Bill is one of the authors on a new paper coming out in the Proceedings of The Royal Society (B), entitled ‘A novel mammalian social structure in Indo-Pacific bottlenose dolphins (Tursiops sp.): complex male-male alliances in an open social network’. The paper is a nice little exploration of the characteristics of social networks in dolphins found in Western Australia; in essence, they were testing whether two hypotheses about the nature of these social networks were tenable given the data they’ve observed. In particular, they tested whether dolphins show signs of engaging in ‘community defence’, where higher order alliances of dolphins form to patrol and defend a larger community range, similar to chimpanzees, or if it follows a ‘mating season defence’ model where male groups shift their defence to smaller ranges or sets of females when it’s mating season. The comparison to terrestrial species with complex social cognition (such as primates and elephants) is an interesting one, because it provides yet more insight into the relationship between the development of complex cognitive faculties and social relationships.

So far, so good. Bill gave a simple explanation of the paper in an email that he was sent out to the E&ERC this afternoon:

We put out a paper that said “dolphin male alliances are not as simple as other species”, but it has stirred up quite a lot of interest, because somewhere in it, the paper mentioned “bisexual philopatry”, which when translated out of jargon means  “males stay near where they were born, AND females stay near where they were born” – nothing more or less than that.

‘Quite a lot of interest’ is one way to put it. ‘Idiots crawling out of the woodwork’ is another. Here’s the headlines of four stories that were written about this paper:

Dolphins ‘resort to rape’: Dolphins appear to have a darker side, according to scientists who suggest they can resort to ‘rape’ to assert authority. [The Telegraph]

Male dolphins are bisexual, US scientists claim. [news.com.au]. (Note that this is an Australian website, and Bill is Australian).

Male bottlenose dolphins engage in extensive bisexuality. [zeenews.com]

And by far the best of the lot (guess who it’s from?):

The dark side of Flipper: He’s sexual predator of the seas who resorts to rape to get his way. [That’s right, The Daily Mail].

……..

Are you kidding me? If the ‘writers’ of these articles had read the paper, they would have noticed that it contains nothing about the sexual behaviour of the dolphins they studied, bisexual or otherwise, aside from brief mentions of the possible consequences of social networks on reproductive success. It certainly didn’t mention anything about bisexual behaviour, homosexual behaviour, or rape. Now, it’s well known that dolphins engage in homosexual behaviours, and I’ve seen papers arguing that they use sexual coercion as well (Rob Brooks confirms this). But these topics have nothing to do with this paper at all. Even a cursory glance through the original source would have killed these headlines – and the first few paragraphs of the Mail story – which aren’t just a miscommunication but border on outright fabrication. The articles themselves are weird mixes of sensationalist headline with a regurgitated paraphrasing of the much better Discovery News piece that they are treating as the primary source. Here’s the problem, though: it’s Discovery News that makes the original mistake about ‘bisexual philopatry’, interpreting it as bisexual behaviour (hot male dolphin-on-dolphin action, as it were). A reporter who had read the original source could have corrected that mistake fairly easily, or could even have been driven to ask further questions. Without that, however, the press cycle grinds mercilessly forward to Flipper the bisexual rapist.

For my part, I was happy to see that James Randerson’s informal survey of science and health writers showed that many of them do read the original papers. And the kind of people who write things about science that I trust, whether they’re professionally trained in science or not, are not the sort of people who do boneheaded things like this. Ananyo might retort that ‘asking questions’ is enough (he suggested as much in his comment above). Matt Shipman said much the same thing in the piece that Ananyo was commenting on. Yet of all people, Ananyo should be wary of this answer, with his focus on investigative science journalism. A scientist writing an email or doing a phone interview can tell you just about anything that you want to hear; a press officer can write a terrible press release; a wire service will probably distort what comes down the line. But a scientific paper is the One, True Source. It is a public record of what was done, and it is the first and best place to start for answers about a study or a scientific topic[3].

Don’t mistake my criticism of Ananyo’s position of reading scientific papers as a general attack on scientific journalism. I think that there’s a lot of great science journalism out there, and that there are even more great science journalists and communicators. Despite the perennial swirl of internet discussion on the topic, I don’t actually think that the whole field is hopelessly broken like some seem to. I just happen to believe that scientific papers, the products of our time and energy as researchers, form an integral part of the process of talking about science (and it’s part of the reason for my support for Open Access publishing). And I think that disgraceful trainwrecks like the reporting on Bill’s paper are a perfect illustration of the need for these papers to be a part of that process.

[Update: Rob Brooks has also discussed this issue over at TheConversation].

——-

[1] Because of Twitter’s space constraints, this was misconstrued to mean that I was agitating for all science journalists to have a Ph.D. in a scientific discipline. Though I wouldn’t be upset if this happened, that’s not what I meant: it is more than possible to have a deep love and knowledge of science without having a degree in a scientific field. Hell, Carl Zimmer probably knows more about viruses and evolutionary biology than I do, and his only training is an undergraduate degree in English. My argument is only that having scientific training increases the probability of a writer or journalist having a good grasp on how science works, not that it’s the only way for that to happen. I will continue to argue, though, that those having a love of science (professional or amateur) will, on average, produce better science writing and science journalism than those who don’t.

[2] He also claimed that most of the people asking journalists to read papers are biologists and medical people, who write easier-to-understand papers. I would have to turn this back on him: if biology and medical papers are so easy to understand, why shouldn’t journalists read them every time?

[3] Yes, there’s no guarantee that what is written in the paper is true. But the chances of detecting fraud are essentially zero if you don’t read the paper to begin with, and if you’re a journalist looking to catch the next Stapel, chances are that you’ll have to wait for the scientific community to find him and tell you about it anyways.

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Group selection, again. Yay.

I was amused to see that David Sloan Wilson took a weird poke at Dawkins, got thrashed by Jerry Coyne, and didn’t like it.  In fact, I was going to leave this as a link post, but while searching for a link to Coyne’s piece (Wilson can’t seem to figure out how to embed links to anything but his own blog in his posts) I came across a post by a blogger who calls him/herself “The Verbose Stoic”.  This piece is problematic on several points, but discussing this is going to take some space so I’ll do it here instead of a comment on Verbose Stoic’s blog;   from here on, I’m going to refer to him/her as VS.

VS starts off by questioning “examples”:

 What I want to talk about is the objections that Coyne raises against Wilson’s group selection theory:

Dawkins’s argument against the efficacy of group selection was that this form of selection is usually unsuccessful because groups are vulnerable to subversion from within by those selfish replicators. That is, “cheating” replicators that are “good” for individuals but bad for the group as a whole will tend to propagate themselves. Yes, altruism may help groups propagate, but altruistic groups are susceptible to invasion by cheaters unless the “altruism” is based on kin selection or individual selection via reciprocity.

That’s the main one, but he goes on to fill in more later:

Dawkins’s (and my) beef with group selection as a way to evolve traits that are bad for individuals but good for groups is that this form of selection is inefficient, subject to subversion within groups, and, especially, that there’s virtually no evidence that this form of selection has been important in nature.

Let me deal with the two minor ones before getting back to the main event. Starting with the last one, we can see that it’s a bad argument, because what Coyne is doing here is saying that one of the reasons to reject the examples Wilson’s giving of cases where group selection has been important in nature is … that you haven’t found examples of cases where it has been important in nature. Except, perhaps, for the specific cases Wilson is citing. You can’t in any way reasonably claim that the fact that you haven’t found examples of it yet means that you can dismiss this proposed example.

Look, Wilson isn’t citing any specific cases of group selection occurring in nature, mostly because there aren’t any.  When I say that, I mean that Wilson hasn’t been able to demonstrate that a trait arose because of group selection and not kin selection or natural selection or any other evolutionary force.  Wilson’s argument is that (1) group selection (a.k.a. “new” group selection or multi-level selection) is something different than any other variety of selection, and (2) that it is responsible for the evolution of traits such as altruism.  But (1) group selection reduces mathematically to inclusive fitness (follow the links in my previous post), and so (2) is trivially true.  Sure, it arose by “group selection”, but that’s an empty statement.  Wilson’s ‘proposed example’ is a theoretical model that was dealt with when he proposed it nearly 40 years ago (Wilson, 1975), and though it’s been refuted dozens of times since, he keeps holding on to it and insisting that he’s already won.   I’ll quote at length from West et al. (2007) to drive home the point:

It has since been shown that kin selection and new group selection are just different ways of conceptualizing the same evolutionary process. They are mathematically identical, and hence are both valid (Hamilton, 1975; Grafen, 1984; Wade, 1985; Frank, 1986a, 1998; Taylor, 1990; Queller, 1992; Bourke & Franks, 1995; Gardneret al., 2007). New group selection models show that cooperation is favoured when the response to between group selection outweighs the response to within-group selection, but it is straightforward to recover Hamilton’s rule from this. Both approaches tell us that increasing the group benefits and reducing the individual cost favours cooperation. Similarly, group selection tells us that cooperation is favoured if we increase the proportion of genetic variance that is between-group as opposed to within-group, but that is exactly equivalent to saying that the kin selection coefficient of relatedness is increased (Frank, 1995a). In all cases where both methods have been used to look at the same problem, they give identical results (Frank, 1986a; Bourke & Franks, 1995; Wenseleers et al., 2004; Gardner et al.,2007).

VS also isn’t happy about “efficiency”:

The first one is also a pretty bad argument when you look at evolution. The argument is that Wilson’s proposed solution would be inefficient, but it seems to me that one of the main thrusts of evolution is that it can indeed be — and often is — inefficient but as long as it works, that’s not a problem. When has it become a criteria for evolutionary explanations that it achieve maximal or even reasonable efficiency. To go down that route would risk re-introducing a need for a designer, to ensure that the mechanisms stayed efficient. That can’t be what Coyne wants. But, again, why is efficiency even a factor? Why would you sort evolutionary arguments by efficiency? Being more or less efficient isn’t a hallmark of evolutionary mechanisms, so if two mechanisms are proposed but one is more efficient than the other that says absolutely nothing about which one is more likely to be true.

Efficiency is a perfectly fine criterion to use, though the term is a little vague as used here.  Assuming that group selection is different from inclusive fitness (which it’s not):  if group selection results in an very slow rate of change in gene frequencies or a lower probability of fixation compared to inclusive fitness, then inclusive fitness is more ‘efficient’ and is more likely to be the cause of a trait fixating in a population.  At least, that’s how I would use the term;  I don’t want to put words in Dr. Coyne’s mouth, though I think that my view here is consistent with his usage and with the literature I’ve reviewed.  In other contexts, I’ve also seen ‘efficiency’ used to say that group selection wouldn’t actually the enhance relative fitness of altruism vs ‘cheating’ (which isn’t a great term for this, as I discuss below), which ends up in the same place.
In any case, VS seems to be confusing efficiency (whether Dawkins / Coyne would use it the way I do or not) with design.  Adaptations are often very badly designed, such as the case of the amazing recurrent laryngeal nerve, but that doesn’t say anything about how fast (or with what probability) genes for those adaptations spread through populations as a result of natural selection.  Even if group selection works the way that Wilson thinks it does, reasoning from the published theoretical models it’s easy to see why it would be an extremely inefficient process with its cycles of groups / reproduction as compared to overlapping generations with continual selection pressures.
VS finally goes onto what he thinks is the biggest error that Coyne makes:

That leaves us with the main complaint: cheaters. The main issue here is that there is an issue raised against the individual selection explanations of altruism as well, even kin and reciprocal altruism and it is … cheaters. Cheaters will benefit if they can get away with it, and so those individuals will prosper and those who are altruistic will be outstripped, and so altruism is not self-sustaining at the individual level. To get around this, the proponents of evolutionary explanations for altruism end up appealing to cheater detection mechanisms […]

Additionally, it seems to me that group selection can actually get this without having to apply specific cheater detection mechanisms. After all, group selection would imply that the relevant competing entity is the group. Thus, if a group has a significant percentage of people who are altruistic, then it outperforms groups that don’t. Thus, if you have a group where this happens and where too large a percentage of the group are cheaters, then that group will cease to get those benefits and be outcompeted and presumably eventually exterminated by the groups where that does not happen. Thus, group selection here becomes self-sustaining; if you are above or at the magical percentage that means you benefit from being altruistic, you benefit over other groups as long as it stays there, but if it ever drops below that your group may well collapse and your individuals, then, all lose. Note that we would still see cheater detection mechanisms emerge because they are mechanisms that make the group stable and so less likely to fall below that percentage and collapse.

It seems like VS might be on the verge of confusing old and new school group selection, as the bolded statements (my emphasis) suggest.  West et al.’s paper has a great figure that shows the difference between the two:

In the text of their article, they point out that “[a]nother way of looking at this is that the new group selection approach looks at the evolution of individual characters in a group structured population, whereas the old group selection approach looks at the evolution of group characters”.  VS’s own words make him sound like a disciple of Wynne-Edwards, which would be unfortunate since Wynne-Edwards was decisively crushed by George Williams in the 1960s.  But even if he’s just poorly recapitulating Wilson’s models, VS is still wrong on the evolution of altruism.  There are a number of possible explanations for altruism, including inclusive fitness, but I don’t want to get into a long conversation on how altruism might have evolved because I would have research and then write an inconveniently long book to do so.

Having said that, Coyne’s use of “cheating” (even in quotations) is a little unfortunate, because it overlaps with the literature on Prisoner’s Dilemma  and cooperation.  Cooperation and altruism are not the same concept (again, see West et al. for a good breakdown of the different concepts, or any text on social evolution);  altruism might be a subset of cooperation, depending on how you define the terms, but usually altruism comes at a cost to the altruist while cooperators do not necessarily pay a cost to cooperate.  “Cheating detectors” is more appropriate for a conversation about cooperation than altruism  (see also Figure 2 of this paper), which makes the rest of VS’s argument difficult to respond to.  I think that Coyne is using ‘cheating’ to refer to individuals who receive the benefit of altruistic acts without paying the price of altruism, but that’s not the same as cheating in models of cooperation.  (Honestly, ‘cheating’ isn’t a great word on a lot of grounds, including confusion with other areas such as signalling and an implication of conscious intent where none is necessary).

Returning to the posts that started this digression:  my honest belief is that this group selection debate should have been over years ago, but I will still support Wilson’s right to continue trying to make his case.  If he’s going to attack people like Dawkins and Coyne, though, he’d better learn to be prepared for them to hit back.  And though it’s unlikely that either of them will ever read this post, I’d like to tell them that they’re not alone.

P.S. Can I take this opportunity to point out a further example of Wilson claiming that people agree with him when they don’t?  If you read the end of Wilson’s second piece, he says:

For readers who are up for a challenge and want to learn more about the theoretical basis and empirical evidence for group selection from someone other than myself, I recommend Steven A. Frank’s “Natural Selection. III. Selection vs. Transmission and Levels of Selection (Journal of Evolutionary Biology, 2011). For Frank, it goes without saying that natural selection is a multilevel process and that the group level is often a significant evolutionary force.

I’ve actually read that paper.  In it, Frank once again points out that kin selection and group selection are the same thing:

The equivalence of r and Hamilton’s formal theory of kin selection establishes the exact equivalence of multilevel group selection and kin selection.

And then, after a long analysis, he compares the usage of the two methods in a section entitled (tellingly): Reasons to favour kin selection over group selection.  It contains exactly what the title says.  If you can get it and you like technical discussions of evolutionary biology, I urge you to read the paper yourself.  If you don’t, then just do me a favour and don’t accept Wilson’s claims about this paper at face value.

——–

David Sloan Wilson. A theory of group selection. Proceedings of the National Academy of Sciences, 72 (1):143–146, 1975.

S. A. West, A. S. Griffin, and A. Gardner. Social semantics: altruism, cooperation, mutalism, strong reciprocity and group selection. Journal of Evolutionary Biology, 20(2): 415–432, 2007.

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It’s true!

As seen on Twitter:

The "what X does" meme for evolutionary biologists...

I really have nothing to add to this...

Also, don’t miss the closely related Scientists version…

Is it the 1960s again?

Ritual Sacrifice of the Gummulate Tribe!

Ritual Sacrifice of the Gummulate Tribe! by Grizdave, used under a CC license

 

Found in a textbook today ([1], p. 14-15), immediately following a discussion of Ebola and Lassa fever infections in humans:

While having the death of a host individual occur as the product of an encounter with a pathogen may seem like a dire outcome, this outcome represents a mechanism of defence operating at the leve l of the host population.  If a particular infectious agent is something against which members of the host population could not easily defend themselves, then it may be better to have that particular host individual die (and die very quickly!) to reduce the possible spread of the contagion to other members of the population.

In other words, if it looks like you’ve been infected by something nasty, you sacrifice yourself to stop its spread for the good of the other members of your population.

Look, I’ll be the first to admit that I hold a dim view of multi-level selection, but I’d be really surprised if anyone in the MLS camp were to make an argument as simple-minded as this.  Virulence is a complex topic, certainly, but the above paragraph could have been lifted from a previously-unknown book by Wynne-Edwards in the 1960s and no one would know the difference.  How is it that people are still getting away with stuff like this forty years after it was first shredded by the likes of George Williams and John Maynard Smith?

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1. Christon J. Hurst. Defining the ecology of viruses. In Christon J. Hurst, editor, Studies in viral ecology, volume 1, chapter 1, pages 3–40. John Wiley and Sons, Inc., 2011.

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What is an animal’s “choice”?

Image by loryresearchgroup

In behavioural ecology, we face a number of limitations in trying to ferret out the relationship between behaviour and evolutionary forces.  These range from the philosophical and theoretical (e.g. what makes a behaviour adaptive or an adaptation?) to the mundane and methodological (is that experimental set up really measuring aggressive behaviour?), and solving these problems is one of the most pressing tasks facing a behavioural ecologist attempting to make useful statements about a behaviour’s evolution.  However, while some of these issues are recurrent and obvious, others are more subtle and can sometimes slip under the radar.  One such problem is the topic of a recent paper by Véronique Martel and Guy Bovin, published recently in the Journal of Insect Behaviour and entitled “Do choice tests really test choice?”  (DOI: 10.1007/s10905-011-9257-9).

The thrust of their argument is that there is a difference between “apparent choice”, and “true choice”, which is driven largely by the fact that we can’t ask animals what they would have done under different circumstances.  As Martel and Bovin point out, animals may make one choice when presented with a particular set of stimuli, or resources as they call it (which may mimic natural conditions!), but express a different preference when presented with a larger set of resources, or when the conditions of the choice are changed.  They distinguish three characteristics of a true choice, only one of which is met by an apparent choice:

  1. The choice must be non-random, i.e. that individuals must choose one resource more often than the others;  testing only this criteria means that researchers are measuring apparent choice, while this is a necessary but not sufficient criteria for true choice.  (I would add to this that the choice probability should be fairly stable if the animal is made to choose under exactly the same conditions).
  2. The choice should be the same even in the “absence of a differential response by the resource” (p. 332). The authors state this to avoid situations in which the resource (e.g. a potential mate) is manipulating the choice of the focal animal, a problem which reminds me very much of the literature on animal signalling.
  3. It should be demonstrated that every resource is perceived, to avoid issues of sensory bias and the like.  It strikes me that this criterion will be hard to meet;  for example, if while testing mate choice the researcher tries to demonstrate a lack of bias by showing responses by the focal individual to each of the potential mates in isolation, how does that prove that one or more of the potential mates aren’t being ignored when the focal individual is given the choice between all of them?
As the authors state, meeting criterion 1 is sufficient for an apparent choice, but 2 and 3 are required for a true choice.  They spend the bulk of the rest of the paper giving examples of both apparent and true choice and elaborating the differences between the two.  It should be noted that they are not claiming that one type of methodology is “better” than the other;  in fact, they take pains to point out the pros and cons of both.  Here’s an example:

The importance of distinguishing between apparent and true choices depends on the objective of a study. If the objective is to establish which resources will be exploited under natural conditions, then the apparent choice is appropriate. If the experimenter wants to know which female will be mated by a male in a natural situation, then the results of this test (the apparent choice) will provide the answer. However, if the objective of the experiment is to establish the mechanisms of this choice, then it becomes important to look more closely at the results. If a male does not perceive a mated female as a resource because she does not produce sex pheromone, the male is thus inseminating virgin females as they are the only resource perceived. In this case, an apparent choice (the virgin female) is expressed, but this choice is the result of the non-perception of the mated female, which prevents this apparent choice from being a true choice. Measuring an apparent rather than a true choice does not remove the relevance of the test, but only modifies its interpretation. Consequently, it is important for the experimenter to state a clear question before identifying the adequate experimental setup to use.

I think that it’s important to mention here that the ideas expressed in this paper aren’t terribly groundbreaking;  a number of people ranging from economics to psychology to behavioural ecology have, at one time or another, made largely the same argument or a variation thereof (one example of a related problem is raised by a really smart guy, Jeffrey Stevens, in this book chapter here).  In fact, I’m a co-author on a paper currently in press at Behavioural Ecology talking about this issue from the opposite direction, wherein we argue that the mechanisms that underlie behaviour may be constrained and that these constraints need to be taken into account when assessing the evolution of behavioural outcomes[1].  I even made an argument very much like the one in this paper during my Ph.D. synthesis exam!

Having said that, I like the paper for its laser-like focus on raising awareness about a very specific part of animal behaviour and cognition that can seriously undercut the conclusions drawn from experimental or field work if the appropriate test isn’t matched to the hypothesis the researcher wishes to explore.  I suspect that their definition of apparent and true choices is incomplete and leaves out issues that will be hashed out in future papers, but if the journey of a thousand steps has to start somewhere, it’s not a terrible first stride.
——–
[1]. I’ll write more about this here when the paper is published.

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Got questions about inclusive fitness?

Over at his blog, Andrew Gelman briefly mentions the recent profile of E. O. Wilson in the Atlantic, and along the way mentions the dustup over inclusive fitness that I may have mentioned here before  (did I? It’s hard to remember).   At the end, he makes a throw-away comment which drove me nuts:

The article also discusses Wilson’s recent crusade against selfish-gene-style simplifications of human and animal nature. I’m with Wilson 100% on this one. “Two brothers or eight cousins” is a cute line but it doesn’t seem to come close to describing how species or societies work, and it’s always seemed a bit silly to me when people try to loop everything back to a selfish-gene story.

I’ve been trying to think of a similarly aggravating comment to make about statistics in return;  maybe “lies, damned lies, and statistics”?  “You can prove anything with statistics”?  “Bayesian statistics suck because I don’t understand where priors come from?”  It bugged me enough that I left this comment:

It doesn’t seem like you know much about inclusive fitness, a theory has been massively successful in evolutionary biology. Despite the odd and unsupported comments made by Nowak et al., it stands firm as a well-supported and useful body of theory. Here’s a link to the letter published in response to Nowak et al.’s original article, signed by 137 authors including most of the field’s brightest minds:

http://www.nature.com/nature/journal/v471/n7339/full/nature09831.html?WT.ec_id=NATURE-20110324

The appeal to authority doesn’t mean that they’re right, of course, but extraordinary claims require extraordinary evidence; Nowak et al. have done nothing but ignore the entire published literature on inclusive fitness spanning decades and comprised of hundreds if not thousands of studies, while proposing a mathematical model that adds nothing to our understanding beyond what current theory already provides.

I respect your work on statistics, have always enjoyed reading your blog, and your book (BDA) is sitting on my shelf right now, but your offhand comment above is uninformed and very aggravating; I’d like to deal with that aggravation by offering to assist you in understanding one of the most powerful explanatory mechanisms in evolutionary biology. The letter above provides a succinct summary of the evidence that Nowak et al. ignore, but it might be a bit much for a non-technical audience; I haven’t published directly in this field, but I do work in evolutionary biology and I should be able to answer any specific questions you may have if you would like to pose them. If I can’t answer them myself, I will find people who can.

I’m not going to go into a full blown recapitulation of inclusive fitness theory and then defend it, because I’d have to write several inconveniently long books to do so.  But since I made the offer over there, I’ll make it here too for any interested readers:  if you have questions burning you up about this whole “inclusive fitness” thing, ask them here in the comments and I will do my best to answer them for you.  And if I don’t know what the answer is, I’ll find it.  No question is too small, though I make no promises on how long or short my answers will be!

I’ll leave off with a quotation from a fantastic book by Andrew Bourke that I’m reading right now, Principles of Social Evolution:

Like any large and active field of investigation, the theoretical study of social evolution is not free from disagreements and unresolved issues (e.g. Taylor and Nowak, 2007; West et al. 2007a).  Paradoxically, while the potential richness of inclusive fitness theory as a general theory of social evolution is still underappreciated, the theory is sometimes perceived as an entrenched orthodoxy. A tendency therefore exists for iconoclastically-minded theoreticians to derive models of cooperation in novel ways and then announce them to be fundamental additions to existing theory (e.g. Killingback et al. 2006; Nowak 2006; Ohtsuki et al. 2006; Traulsen and Nowak 2006).  It is healthy for orthodoxies to be continually challenged by new theories and new data.  However, to date, these models have fallen short of true novelty, as other authors have shown that their results are capable of being derived from inclusive fitness theory (e.g. Grafen 2007a, 2007b; Lehmann et al. 2007a, 2007b; West et al. 2007a).  Indeed, inclusive fitness theory has a long history of successfully assimilating apparent challenges and alternatives (Grafen 1974; Queller 1992; Lehmann and Keller 2006a).  This is not surprising when one considers its deep foundations in the theory of natural selection.  Although it is premature to declare a consensus, a substantial body of opinion therefore holds that claims of fundamental extensions to inclusive fitness theory will have to be radically innovative, as well as robust, to be accepted as such (e.g. Lehmann and Keller 2006a; West et al. 2007a).  For all these reasons, Hamilton’s (1964) inclusive fitness theory will underpin the conceptual reasoning employed throughout this book (pp. 22-23).

 

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Death in the nest: trade-offs rule the day.

Underlying many research programs in biology is the meta question: why is there more than one type of X?  (In continuous form, why is there variation in X?)  This question recurs in many areas of animal behaviour, and indeed in the entirety of the study of evolution itself.  Some examples include:

  • Why do animals show variation in “personality” – why are some consistently more aggressive, more exploratory, bolder, etc.
  • Why are there more than one type of male that females select between?  Why are some “attractive” and others “unattractive” – why aren’t they all attractive? (Sexual selection).
  • If aggressive signals like roaring can make other animals give up a resource or back down from a fight, why don’t all animals use the aggressive signal?  Why is there variation in signal type when all animals should use the same signal, which would then lose all meaning and be ignored?
  • Why do some animals invest heavily in each offspring while others produce as many as they can and invest very little in each?
The general response to most of these questions hinges on the idea of a trade-off.  In its most basic form, a trade-off involves giving up one thing to get (or avoid) another.  In particular, animal behaviour often hinges on cost-benefit tradeoffs.  It is desirable to have some trait or perform some behaviour, but doing so may come with a cost if we have too much of the trait or perform the behaviour too often or at all.   Examples of this litter the pages of any textbook in the biological sciences, from molecular biology up to zoology and ecology;  in particular, we can begin to address the questions I listed above by appealing to trade-offs:
  • Some personality types, like aggressive or exploratory, can confer benefits – such as always winning fights or being the first to find food – but also come with costs – such as the injuries from always fighting or the cost of being eaten while you try to be the first to eat.  Some individuals will be willing to make this trade-off, others will not.
  • The answer to this question has filled entire bookshelves, but here’s one tiny example:  in 1975, Amotz Zahavi published a landmark paper proposing that attractive males are “handicapped”;  they willingly trade off the cost of the handicap for the increased number of matings of come with it.  Zahavi’s “handicap principle”  suggested that this was a reliable indicator of quality to females because only some males would have the required quality (be strong enough, fast enough, etc) to bear the cost of the handicap in order to reap the benefit.
  • One of the most well-known answers to this question began the field known as evolutionary game theory;  at the end of the 1970s, the tragic figure of George Price and the eminent John Maynard Smith answered the question by showing mathematically how frequency-dependence could lead to a trade-off between Hawks, who are aggressive, and Doves, who back down at the first sign of trouble;  when Hawks are extremely common, their aggression leads them into costly fights against each other, which reduces the benefit of aggressiveness and makes Dove-ish behaviour more attractive.  But when Doves are common, Hawks get immense benefit with no cost by bullying Doves around.  (There’s actually significant overlap between this point and the previous, but that’s a topic for another blog post!)
  • An entire branch of evolutionary biology, life history theory, deals with questions like this:  in the face of limited resources, how do individuals make choices about the timing and sequence of events in their life to maximize their fitness?

This general pattern underlies the story behind a neat new advance-access paper from the groups of Alex Kacelnik and Juan Reboreda that manages to give away the good stuff in the title:

Ros Gloag, Diego T. Tuero, Vanina D. Fiorini, Juan C. Reboreda, and Alex Kacelnik. The economics of nestmate killing in avian brood parasites: a provisions trade-off. Behavioral Ecology, 2011.

Here, the question of types and the answer of trade-offs arises in the context of brood parasitism.  Brood parasites are organisms – birds, fish, insects – that relieve themselves of the responsibility of parenthood by tricking other organisms into doing it for them.  In birds, this usually takes the form of brood parasites laying their eggs in other species’ nests, where the enterprising young tykes then pretend to be the offspring of the unlucky suckers who are to play host.  Brood parasites can be specialists that only parasitize the nests of a target host species (or small group of species); an example of this is village indigobirds, who generally parasitise fire-finches (and who also display an interesting mechanism where the young copy the songs of the host species).  Generalists, on the other hand, will parasitise a range of host species;  cowbirds, for instance, are generalists.  Brood parasites can also vary in whether they eliminate the other offspring of the host that they have colonized (nestmate killing) or whether they attempt to blend into the crowd (nestmate tolerant).  To make this more concrete, take a look at this short video showing a newly-hatched cuckoo ejecting a reed warbler chick from the host nest:

The paper I’m talking about here explores an interesting question about brood parasites, namely:  why are some brood parasites nestmate tolerant while others are nestmate killers? Gloag et al. propose a mathematical model that explains this in terms of a “provision trade-off”.  Host nestlings can help the newborn parasite by stimulating the host parents to bring more food than the parasite could solicit alone, and if the parasite can outcompete its nestmates for that additional food, then it does better to let them live.  Thus the trade-off:  when the host offspring increase the fitness of the parasite, it lets them stay, but otherwise it kills its flatmates.  Gloag et al. take the time to break this trade-off down into its constituent parts, namely (in their words, p. 2):

  • The total provisioning rate stimulated by the whole brood, and
  • The share of the provisions received by a parasite nestling.
The simple model they derive shows that when the ability of a parasite to stimulate food provisioning by the host parents is greater than its ability to compete for food with its nestmates, the parasite will do best if it is reared alone and the murder spree begins.  This relationship depends on the interaction between these two variables;  in other words, “[i]f each host nestling causes a greater increase in provisioning than the amount it consumes, then the presence of host chicks would result in higher consumption for the parasite, even if a host chick takes a bigger fraction of the extra food than the parasite.”  The model helps to predict where each scenario – nestmate killing or tolerance – is plausible as a function of this intuitive trade-off.
VIRA-BOSTA (Molothrus bonariensis)

VIRA-BOSTA (Molothrus bonariensis) by Dario Sanches, on Flickr

Gloag et al. then use this model to explain differences not only intra-specific differences between specialist species in their level of nestmate tolerance, but also inter-specific differences within generalist species as well.  This would have been a good paper even if they had stopped there, but they then go on to test their ideas in the field using a generalist parasite, the shiny cowbird (Molothrus bonariensis). Working in South America, they searched for the nests of two types of shiny cowbird hosts, chalk-browed mockingbirds and house wrens, and set up two experimental conditions.   In the “mixed group”, the a single cowbird egg was placed among host eggs, and in the “alone” group, the cowbird eggs were placed in the host nest with dummy eggs so that the cowbird young would be reared alone.  They measured the food amount and quality brought to the nest from video recordings, and measured the physical quality of the resulting offspring (weight and tarsus length).  They also compared the mortality rates of the cowbird chicks to see if there was a difference between the conditions.  Their findings?

In our field study, nestmate tolerant shiny cowbirds encountered both sides of a provisions trade-off depending on the host used. When reared by chalk-browed mockingbirds, nestling cowbirds had higher food consumption, mass gain, and survival when alone in the nest than when sharing with 2 mockingbird young. In contrast, cowbirds reared in the nests of house wrens had higher food intake and growth when reared alongside 3 or 4 host young than when reared alone. (p. 7).

The results of their work suggest strongly that there is a trade-off at work here, and that the virulence of parasite offspring will be affected by the provisioning characteristics of the host environment.  Of course, they are quick to suggest that there are other factors potentially at work in differential growth rates, such as thermoregulation (larger broods can help each other thermoregulate) or size of the nestlings.  Nestling size is an interesting issue, because as the authors mention, cowbird young are larger than house wren nestmates but equal in size to or smaller than their mockingbird counterparts.  This may the competitive ability of the young either through physical competition between nestlings where size would be important, or because parents preferentially feed larger offspring.  (As a by-product, this also raises the longer-standing question of why host parents don’t do a better job at discriminating among their young for parasites in the first place;  for an explanation in terms of yet another trade-off, I’d refer you to this letter to Nature by Arnon Lotem as a possibility).

Wilson's Warbler feeding it's Cowbird chick  "offspring"

Why are you feeding this monster? (by Alan Vernon, on Flickr)

The work on trade-offs in this paper provide a simple and intuitive model for the action of brood parasites across a wide variety of situations, and then back it up with empirical data that demonstrate this trade-off in action.  It’s hard to ask for more from a paper!  Of course, as with every paper you’ll ever read, “more research is needed” (we have to say that, or we’re straight out of a job, aren’t we).  It wil be interesting to see if this trade-off does actually hold in other species, and combining the principles in this paper with a phylogenetic analysis would make for a fascinating approach. In the meantime, though, if you’ve read this far I’d urge you to take the lesson of this paper to hear and learn to look for the trade-offs inherent in many biological systems.  As a guiding principle of biology, I guarantee that you’ll see it almost everywhere you look.

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Group selection a done deal? Hint: no.

The modern theory of natural selection derives...

Image via Wikipedia

In reading Jerry Coyne’s review of David Sloan Wilson‘s new book, The Neighborhood Project, I came across this succinct summary of what I agree is the current feeling on group selection:

Group selection isn’t widely accepted by evolutionists for several reasons. First, it’s not an efficient way to select for traits, like altruistic behavior, that are supposed to be detrimental to the individual but good for the group. Groups divide to form other groups much less often than organisms reproduce to form other organisms, so group selection for altruism would be unlikely to override the tendency of each group to quickly lose its altruists through natural selection favoring cheaters. Further, we simply have little evidence that selection on groups has promoted the evolution of any trait. Finally, other, more plausible evolutionary forces, like direct selection on individuals for reciprocal support, could have made us prosocial.

These reasons explain why only a few biologists, like Wilson and E. O. Wilson (no relation), advocate group selection as the evolutionary source of cooperation. […]

At least, this agrees with my reading of the literature;  I’m hardly an expert in this area, but I’ve been swayed by the writings of people like Coyne and the pair of Stuart West and Andy Gardner (e.g. this paper, if you can get it;  this video is also well worth watching).  And nothing D.S. Wilson has ever written has convinced me otherwise.  Thus, I was especially surprised when I picked up a free copy of New Scientist from the Ultimo Big Night of Science – which, incidentally, was fantastic –  and saw that they had published an 8-page hatchet job (which is behind a paywall online here) by Wilson in which he claimed that group selection (a.k.a. multi-level selection or MLS) “is firmly re-established” in evolutionary biology.    “Today, though,” he writes, “there is near-universal agreement among those familiar with the subject that the wholesale rejection of group selection was mistaken and that the so-called alternatives are nothing of the sort” (p. viii).

One of the biggest problems with group selection is that it’s mathematically equivalent to other, better explanations of evolution like kin selection.  Wilson knows this:  he rather transparently tries to co-opt the criticism in the paper by stating it as though it works in reverse (“In addition, it has become clear that the supposed alternatives for the evolution of prosocial behaviour are actually equivalent to group selection”).  In what I consider a despicable move, he even quote mines Andy Gardner:  “‘Everyone agrees that group selection occurs,’ stated evolutionary biologist Andy Gardner in 2008.”  But it’s instructive to look at what Andy Gardner actually said, in this 2008 Nature summary of the ‘debate’:

 “Everyone agrees that group selection occurs,” says Andy Gardner of the University of Edinburgh, UK. Yet Gardner and his colleagues Stuart West and Ashleigh Griffin have trenchantly criticized David Sloan Wilson’s arguments on this subject — a critique to which David Sloan Wilson responded by initiating a lengthy debate in the community under the heading ‘If the theorists cannot agree…’.

Wilson leaves off the part where Gardner and his colleagues don’t agree with him at all, which is a favourite tactics of creationists.  I’ll leave the implication of that up to the readers.

So if everyone agrees that the two are mathematically the same, why not use group selection?  I’ll highlight the strong argument made by West, Griffin, and Gardner which you can read here.  In responding to Wilson’s critique of an article that the authors wrote, West et al. point out three things (p.376):

  1. “No group selection model has ever been constructed where the same result cannot be found with kin selection theory.”
  2. “The group selection approach has proved to be less useful than the kin selection approach.”
  3. “The application of group selection theory has led to much confusion and time wasting.”

If you’re interested in this issue, I urge you to read the linked PDF and follow up with some of the references they give.  I don’t know of clearer writers on this subject, and it’s a great place to start.

I disagree with a lot of what D. S. Wilson writes, but I respect his right to hold the opinions and his efforts to prove his position right.  That’s how science progresses, and if he can ever come up with some strong evidence for his position (which I don’t believe that he has yet), I’ll take a good hard look at it and make up my mind anew.  Until then, though, I would take him much more seriously if he would stop with the claims that everyone agrees with him when they obviously don’t.

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The Nowak controversy resurfaces…

Over at Boing Boing, Maggie Koerth-Baker takes up the issue of eusociality in insects that Martin Nowak and E.O. Wilson (and Tarnita, though she doesn’t get much attention when this issue is raised – I wonder if that makes her happy or sad?) raised such a hullabaloo over last year.  If you’re new to the issue or just enjoy good science writing, it’s well worth reading all the way through.  My own perspective?  I’m with most of the field in thinking that Nowak et al. were out to lunch on the evidence for kin selection, and as to whether group selection is in operation … well, let’s just say that I found this talk very convincing (h/t for that to Jerry Coyne).

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Gay zebra finches, oh my. Oh, wait…

Taeniopygia guttata (Zebra finch)

Image via Wikipedia

I’ve seen this paper about strong homosexual pair bonding in zebra finches pop up in a couple of places around the web, but it only really caught my eye when I read Carin Bondar’s somewhat breathless report on the matter entitled “The astounding strength of homosexual bonds in Zebra Finches: Ladies need not apply…”.  In essence, the researchers discovered that when you manipulate the sex ratio of zebra finch groups to be male-biased, male pair bonds form that display all of the same behaviours that female-male pair bonds do, and that when females are later reintroduced to these homosexual pair bonds, the male pair-bonds don’t break up.

It’s an interesting paper, and the findings are, well, pretty cool.  But I have to disagree – respectfully – with Dr. Bondar’s assessment of the startling nature of these results.  First, given that zebra finches tend to mate for life anyways, the finding that male-male pair bonds are strong shouldn’t come as a surprise if you think mechanistically.  In fact, I think it would have been a lot more surprising if the male-male bonds had been of a different quality;  if you think through the evolutionary implications, having a different mechanism for male-male as opposed to male-female bonds would imply that selective pressures on these types of bonds was different for some reason, and would really beg the question of why.  Instead of a single ‘mating’ mechanism (a combination of hormones and neurobiology among other things, which I’ll touch on again in a moment), this ‘conditional’ pair bonding would require either a single mechanism with an unintended consequence, or two separate mechanisms, one for male-male bonds and one for male-female.  That’s not out of the question, certainly;  many potential explanations for same-sex sexual behaviour in animals imply such mechanisms.  But to me, having a life long pair bond with females and then an entirely separate short-term pair bonding mechanism for male-male interactions would need explanation.  Indeed, as Dr. Bondar’s own blog post notes, “homosexual couples both COURTED and COPULATED with each other”;  even if homosexual pairings are adaptive (as they might well be!), it seems odd to waste even a little energy on copulation and suggests a single mechanism or set of mechanisms at work.

Second, it was already established that there are both hormonal and social / developmental mechanisms affecting same-sex preferences in zebra finches;  in particular, Elizabeth Adkins-Regan did a lot of work from the late 90s onwards on both of these mechanisms (and her student, James Goodson, has done a lot of great follow-up work on mapping the endocrinology and neurobiology of social behaviour in estrildid finches).  The finding in the article by Elie et al. that biased sex ratios promote homosexual pair bonds is interesting, but I wonder how different it is from the social deprivation work by Adkins-Regan and her collaborators.

Don’t get me wrong:  this is a cool article.  It deserved to be published, and it seems to make a couple of important contributions- exploring and quantifying the strength of these bonds was a worthwhile task, and the evidence it provides for the “social partner hypothesis” is worth looking at.  But the media has, as per usual, gotten most of the story wrong here (for instance, the BBC Nature story made it sound like the paper was the first to establish same-sex bonds in zebra finches – <sigh>), and while I share Dr. Bondar’s interest in the results, I don’t think that they’re nearly as shocking as she does.

As a postscript to this:  at the end of her article, Dr. Bondar says:

 However, long term studies will shed light on whether males will seek out females for the sole purpose of genetic propagation outside of their homosexual partnerships.  For the sake of their evolutionary future I hope they do :)

I’m not aware of anyone having tested this specifically.  But it’s been known for a long time that zebra finches engage in a fair amount of extra-pair copulating (i.e. they’re socially monogamous, but not sexually monogamous), so I would expect that the males are stepping out to enhance their reproductive fitness.

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