Book Club: Darwin’s Unfinished Symphony, 3, fish tales and creativity

Threespine and Ninespine sticklebacks

Continuing our discussion of Kevin Laland’s Darwin’s Unfinished Symphony, on the evolution of culture, I am going to briefly cover “A tale of two fishes” (ch. 4) and “The roots of creativity” (ch. 5). Together with the chapters we have already discussed, they complete the first part of the book, devoted to the foundations of culture. (After this, we’ll move to the chapters in the second part, on the evolution of the mind.)

Chapter 4 is devoted primarily to research conducted over a period of two decades by Laland’s own lab, focusing on the contrast in the behavior between two small species of fish, the threespine and the ninespine sticklebacks. The reason for working on this sort of experimental animals is that if one is interested in social evolution then one needs to set up replicates of entire populations. Logistically, this is going to be impossible to do for large vertebrates, especially mammals, but it is eminently feasible with fish. Sticklebacks are a well studied group of 16 related species, common in rivers, streams and coastal regions of the Northern hemisphere. Evolutionarily speaking, they are closely related to seahorses.

Laland’s lab focused on sticklebacks’ use of public information, i.e., on how they socially learn from other members of their own or even of other species. When they started the research project, the consensus was that use of public information required a high degree of intelligence on the part of the animal. It turns out that was definitely not the case, thus providing another important piece of the cultural evolution puzzle. Chapter 4 details lots of fascinating experiments with these two species of sticklebacks, but I will summarize only the basic stuff, leaving it to the interested reader to dig deeper.

The basic setup is one in which an aquarium is divided into compartments. In one area some fish of either species are being fed at a high rate (“rich patch”); in a second one they are being fed at a lower rate (“poor patch”); and in a third one they can observe their fellow species members feeding before being allowed to do so themselves: “if the sticklebacks were capable of public-information use, they would be able to distinguish between the rich and the poor patch based solely on the reactions of the demonstrators to the food.” (p. 80).

Interestingly, the ninespine was apparently able to use public information and, when allowed access, swim preferentially to the rich patch. The threespine, by contrast, showed no preference, indicating that the observers in that species had not learned from the demonstrators. Why the difference?

Laland’s group performed several follow-up experiments aimed at eliminating a number of simple explanations, such as that perhaps the demonstrators of one species were not as good as the demonstrators of the other, or that there was an inter-specific difference in the visual acuity of the fish, or maybe some of the relevant cues were olfactory, not just visual. None of that was the case.

“We began to believe that what we had discovered might genuinely be an adaptive specialization in social learning, with ninespines capable of exploiting public information, while their close relatives, the threespines, were not.” (p. 81)

The answer turned out to have to do with the relative cost of social and asocial learning. The cost of asocial learning is different for the two species, because of differences in their anatomical structures. The threespine stickleback has large spines, which are very effective against predation, so much so that often the fish gets stuck into the predator’s mouth, and is forcefully rejected instead of being eaten. This is not the case with the ninespine stickleback, whose spines are more numerous but much smaller and less robust, and therefore not as effective an anti-predator device. Threespines don’t need to engage in public information use because they can afford to explore the various patches and learn on their own. That approach, by contrast, is very dangerous for the ninespines, which accordingly evolved the more advantageous habit of learning socially by observing others. Interestingly:

“The ninespines’ behavior is precisely that predicted by a sophisticated evolutionary game theory analysis conducted by an economist in order to understand human behavior.” (p. 89)

Moreover, comparative research conducted on 50 populations sampled from 8 species belonging to 5 genera showed that only the ninespine and their closest relative, the brooks sticklebacks, are capable of public information use, thus demonstrating the intricate relationship between evolutionary history, ecology, and morphology in shaping cultural evolution.

Chapter 5 of Darwin’s Unfinished Symphony opens with the classic example of animal learning and cultural spreading: the invention of a method to open home delivered milk bottles by blue tit birds back in 1921 England. The instance is well documented, and because of the involvement of amateur ornithologists, we know how quickly and how far it spread, eventually to involve several species other than the blue tits. Interestingly, the “invention” appeared to be relatively easy to come by, so that a number of animals arrived at the same solution independently, not necessarily relying on copying public information. So milk bottle opening is a good example of innovation, the devising of a solution to a new problem posed by the environment.

Things like the milk bottle opening clearly show that human beings do not have a monopoly on creativity, though Laland immediately qualifies this by remind his readers that:

“A vast difference exists between dipping food and inventing a microwave cooker, while banging cans together to send a message is a long way from developing e-mail.” (p. 100)

Still, studying innovation is crucial to understanding human creativity and cultural evolution, and it is not easy because it is difficult to recognize a behavior as innovative unless one has a solid baseline of studies on pre-innovation behaviors in whatever species of interest.

One of the classical studies on animal innovation was conducted by Edward Thorndike at Columbia University. He confined cats in small boxes from which it was difficult, but not impossible, to escape. This was something the cats clearly disliked, to put it mildly. Thorndike was able to show that cats — once they learn how to get out of the box — fine tune their behavior so that the escape becomes easier and easier. The interesting part was that the animals arrive at suitable solutions by trying out a bunch of seemingly random moves, until something happens to work, even sub-optimally. It’s innovation by trial and error, very much something human beings do quite well.

One of the most interesting things about this chapter is Laland’s detailed presentation of evidence that, as the saying goes, “necessity is the mother of invention,” meaning that innovations are triggered by new challenges faced by animals, often under unusual or novel environmental conditions. Moreover, studies in callitrichid monkeys clearly showed that it is often the older, more experienced, individuals that come up with innovative behaviors, not the young ones, who are presumably insufficiently experienced to have mastered the problems posed by their environment.

While experiments with mammals, and especially primates, are of course the most fascinating, as pointed out above, they are both logistically challenging and expensive. Hence, again, the use of fish, which are much easier to raise and manipulate in statistically sufficient numbers.

Laland then describes a series of experiments his lab has conducted on another common fish, familiar to aquarium enthusiasts: guppies. The results were fascinating:

“Innovators were significantly more likely to be females than males, more likely to be food deprived than not, and typically smaller rather than larger fish. … The observed patterns are best explained by differences among fish in their motivational state. The first individuals to solve the [problem posed by the experimenter] are those driven to find novel foraging solutions by hunger, or by the metabolic costs of growth, or pregnancy [hence the predominance of females among innovators].” (p. 112)

Research on birds yields equally tantalizing clues. For one thing, species of birds that are more capable of innovation tend to be the ones whose populations survive when introduced into a new environment. Moreover, migratory species are less likely to be innovators than non-migrant ones, apparently because they are not as capable of introducing innovations in order to cope with their environment. If you can’t thrive in a given place, then change place, seems to be the idea. So migration turns out to be an evolutionarily alternative strategy to the option of staying and coping + innovating. Finally, innovative species of birds are more likely to speciate, i.e., to give origin to new species.

Though it is difficult to carry out systematic experiments on primates, it is possible to canvass the extensive literature on primatology, searching for and categorizing examples of innovative behaviors. Laland did this with one of his collaborators, Simon Reader. They found that:

“Consistent with our hypothesis that necessity was the mother of much animal innovation (derived from our fish experiments), across all primates [we] found more reported incidences of innovation in low-status individuals and fewer reports of innovation in high-status individuals than expected in either, given their numbers in the populations. … [We] found that approximately half of the instances of innovation that had taken place among primates had followed some sort of ecological challenge, such as a period of food shortage, a dry season, or habitat degradation.” (pp. 116-117)

And here is the kicker: controlling for phylogenetic relatedness, there is a very strong correlation between a tendency of a species to innovate and both its relative and absolute brain size. This, however, led to a puzzle: while the obvious conclusion to be drawn is that intelligence (measured by brain size as a proxy) has been favored in certain lineages in order to facilitate social learning and innovation, it is also true that several small-brained species — from fruit flies to fish — are capable of both. Why, then, evolve large brains to begin with? That’s going to be the next topic, in the second part of the book.

13 thoughts on “Book Club: Darwin’s Unfinished Symphony, 3, fish tales and creativity

  1. SocraticGadfly

    Thought on migratory vs non-migratory birds — maybe it’s not so much that migration is simply an alternative strategy, but that, per things that you’ve mentioned before, and I have, about evolutionary directedness and energy wells, that, once a species of bird goes down that strategic road, it’s locked in due to amount of brain configuration, energy commitment, and an energy well that’s too high to easily escape?


  2. brodix

    It does seem like what would be called common sense in people.

    Positive and negative feedback, aka, good and bad. The basis of thought.


  3. Robin Herbert

    I haven’t read the book yet so I will have to follow the description for the time being.

    The last sentence, why evolve such large brains to begin with also occurred to me, so I will await the next chapter with interest.

    Copying wouldn’t require so much brain power per se, but identifying a member of your own species to copy would.

    Innovation, on the other hand, could exist in quite simple organisms. Even something with rudimentary sensory organs and a handful of neurons (or even just a network of ordinary cells) can do some rudimentary innovation.

    For example an organism that has a “move when movement is detected” behaviour could in principle change to “don’t move when movement is detected” without this having to be encoded in DNA.


  4. saphsin

    “Innovation, on the other hand, could exist in quite simple organisms. Even something with rudimentary sensory organs and a handful of neurons (or even just a network of ordinary cells) can do some rudimentary innovation.”

    Really? I don’t think so, unless you narrow “innovation” enough to just mean finding ways to respond to a new environment.


  5. synred


    Sally the cat (“the dog chaser”) did something that looked like an attempt to copy us. Our front door in our Palo Alto house had a Euro style handle rather than a knob. There was a table next to it usually covered in junk.

    Sally would jump up on the table and push down on the handle with her paw as if trying to open the door. The handle was attached to a a lock and the action was too stiff for her to force it down even if she’d hung all her weight on it.

    She never got the door open, but every now and then would get up there and try again. It looked like she was trying to copy us.

    Well N=1, etc.


  6. Robin Herbert


    Really? I don’t think so, unless you narrow “innovation” enough to just mean finding ways to respond to a new environment.

    Or new ways to respond to an existing environment. I don’t see how that differs from the way it is used in the guppy example.


  7. Massimo Post author


    “Really? I don’t think so, unless you narrow “innovation” enough to just mean finding ways to respond to a new environment”

    That’s pretty much the definition of innovation in biology, with the caveat pointed out by Robin that it actually applies also to non-novel environments. How else would you define it?


  8. darwinsunfinishedsymphony

    I see some debate on what counts as an innovation. This is not surprising, as it has been a point of discussion within the animal behaviour literature too. Most researchers define innovation as the devising of a novel solution to a problem, or a new way of exploiting the environment. However, on practical grounds and with caveats, we generally impose the requirement that the novel behavior should exhibit evidence of learning to qualify as innovation, rather than just treat any accidental or idiosyncratic action as innovative.
    Oftentimes our first impressions can mislead. For instance, one of the most famous animal innovations is the ‘invention’ of sweet-potato washing by a Japanese macaque called Imo. This impressed because, when it was reported in the 1960s, washing food prior to eating it appeared to be a remarkably sophisticated (indeed, human-like) act for a monkey. Ed Wilson and Jane Goodall described Imo as “a monkey genius” and “gifted”, respectively. Subsequent study over the next few decades established that food washing is a common feature in the behavior of several macaque species, and that all Imo had done was apply an established behavior pattern to a new food. Armed with this background knowledge, Imo’s invention still qualifies as an innovation by my definition, but it illustrates some of the pitfalls of this field, for instance, how this case would have been mischaracterized had the definition of innovation stipulated that some level of complex cognition must be involved.

    When I first began studying animal innovation, I took the line that a broad definition was useful at what was an early stage in the development of the field, as it would encourage data compilation, but that subsequently it might be useful to distinguish between classes of innovation. Recent data bears this out. For instance, some animal innovations comprise no more than the adoption of a novel dietary element. The extreme example that makes the point is the habit of some corvids of eating human vomit (yes there is a scientific study of this, and yes in one North American university the students apparently get drunk and produce vomit with such reliability that it has become a central component of the local bird’s diet). Other cases, known as ‘technical innovations’ involve tool use and/or the extraction of food from a substrate (for instance, the invention by some orangutans of a convoluted procedure for extracting palm hearts from trees with vicious defenses such as sharp spines and knife-edged petioles).

    What is interesting here is that when we apply statistical (i.e. comparative phylogenetic) tools to data from nonhuman primates we find a much stronger relationship of brain size with rates of technical compared to nontechnical innovation. When it comes to primate brain evolution, it would appear that not all innovations are equal. This makes sense. Devising a new means of extracting a food from a protected substrate may require some intelligence, conversely how smart do you have to be to eat vomit! We will see in later chapters that there are reasons for thinking that the relationship between innovation and brain size is a causal one, and that innovation (along with social learning) may have been a driver of brain evolution.

    Liked by 6 people

  9. SocraticGadfly

    Thanks, Kevin. Per previous discussion here, a fair amount by me, about doing a twist on Jaynes and seeing language as the key to purely human consciousness, with everything that entails — including human-level social learning — hoping to hear more from you in coming sections.


    Oh, and were those college students drinking …

    Wait for it, wait for it …

    Old Crow?


  10. Bunsen Burner

    I’m trying to understand the mechanisms involved in the stickleback example. These species are very closely related from an evolutionary viewpoint. Yet one is capable of social learning and no the other? Given that there are many different species capable of social learning does this mean that the genetic mechanism for social learning is constantly being rediscovered, or that there exist multiple different mechanisms of social learning?


  11. Massimo Post author


    “Mechanism” is a fairly flexible word here, and Kevin’s work does not deal with the low-level, chemical-molecular mechanisms of these behaviors. But yes, the ability for social learning evolved several times independently, and likely the underlying mechanisms are different, though to what extent is an open empirical question.


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