A Dialectical Future for Behavioral (and Evolutionary) Ecology: transcript

(this is an approximate transcript for a talk published in a separate post; my formatting was being weird, hence the separate post!)

Thank you all for being here. My talk today is titled “A dialectical future for behavioral ecology,” though I think much of what I’m saying applies to evolutionary ecology as well, I’m going to focus on the study of animal behavior in natural contexts.

I think this talk is likely different than a lot of talks you’ve seen in your departments or even at the Miller, but it’s motivated by two things that we all agree on: first is that we all agree that interdisciplinary work is valuable. The whole reason we come together here at the Miller at these lunches is to find connections across disciplines, and my goal today is to stretch how you think of interdisciplinarity a little bit. And second is this idea that I believe all of us in this room will find intriguing, which is: how can we think in new and different ways in science?

In this talk, I’m going to consider that one way in which we can shift into new modes of thinking in science is by asking fundamentally different questions, which of course then prompts the question: “how do we ask different questions?” And that is the subject of my talk today.

Specifically, I am starting from something called “standpoint theory”, which is rooted in feminist and Marxist ways of thought and makes explicit the role of politics in how we construct knowledge. What I mean here by politics is “the total complex of relations between people living in society”, which includes but is not limited to what you likely think of when you hear the word ‘politics.’

 So what is a standpoint? A standpoint is a way of looking at the world that emerges from involvement in collective political struggle against a dominant perspective. Engaging in political struggle against a dominant narrative allows one to really see aspects of human social relations or the natural world that are not easily accessible from dominant perspectives. Standpoints reveal new ways of looking at the existing questions, and thus generate different questions.

Part of the reason I study animal behavior is because it a particularly interesting place in which to look at the impact of scientific narratives that align with and push back against dominant political narratives. We ask questions about animals, and the answers directly impact what we think of as ‘natural’, and we use that sense of what is ‘natural’ to shape how we think about ourselves, our relationships, and how our societies work. BUT if the questions we ask are themselves shaped by dominant cultural and political narratives and closed off to other possible ways of describing nature, then what we’ve ended up doing through our science is simply legitimizing dominant narratives.

In this talk today, I’m going to tell you first tell you about the dominant narrative in my field of behavioral ecology, which is that of adaptationism. I’m then going to give you an example of what it looks like to push back against that dominant narrative from a collaboration I was part of that was published in 2019, and finally, I’m going to explore where this dominant narrative may have come from politically, and what an alternative to it might be. 

So in the field of behavioral ecology, the dominant framework within which we ask questions is the framework of adaptation by natural selection. Just so we’re all on the same page, here’s a definition that I’ve pulled from the national geographic website, which is that adaptation is any heritable trait that helps an organism survive and reproduce in its environment. And just a bit of jargon that’s helpful to know, which is that we biologists refer to the aggregate of survival and reproduction as “fitness”, and when we talk of costs and benefits of traits in this context we mean, does this trait impact fitness negatively or positively.

Adaptation, of course, is a hugely important force that shapes our natural world, and is the subject of a tremendous amount of research. And I want to emphatically say, I’m not pushing back against adaptation in this talk. What I’m pushing back against is the notion of adaptationism, by which I mean a way of studying nature that centers the role of adaptation in shaping natural variation, a way of looking at the world through a lens where adaptation matters more than any other process.  

When we do work in behavioral ecology from an adaptationist perspective, we start by finding an interesting trait out in nature, say this throat fan on a lizard, and then asking “In what way might this trait be an adaptation? In what way might it be maximizing individual fitness? What are its costs and benefits in the currency of fitness” And then you collect data and ask, okay, do the data match our expectations of what we think should be happening if this trait is an adaptation. And if we find that they match, we are satisfied that we have understood how the trait evolved because we have found an adaptive explanation for it. And if we find a gap here, that’s a puzzle, that’s a paradox—we ask, well how did this trait evolve if it is not adaptive? And then in response to this paradox,  we either say, well we must be misunderstanding the costs and benefits here, so let’s elucidate them a bit better and revise our understanding of what should be happening, or else, there must be other forces of nature—things like random genetic drift, or stochasticity, or phylogenetic constraint, or physiological constraint, or simply heterogeneity that is too complex to wrap our heads around—and these forces are preventing the expression out there in nature of this fitness maximizing adaptive optimum that we think should be happening.  

And so the point here is not that we never consider things other than adaptation in the adaptationist programme. We do. The point is where and how do these other things show up in our narratives, in relation to adaptation?

When we view nature through this adaptationist lens, our image of nature is defined by a notion of what should be happening that is derived largely from the logics of fitness maximization coupled with just enough natural context to make a prediction that seems sensible. And when we juxtapose this image of what should be onto what is, it looks like our image of what should be happening is obscured by all these other things. And then when our image of what is doesn’t match what we expect to see, it’s almost like we try to polish the lens further, and move it closer or further away to better get the two images to match, but we forget that we are looking through a lens, and that lenses can not only magnify and clarify what we see but also distort it.

And the way in which this distortion produced by the adaptationist lens becomes clear is by focusing on the gap between what should be and what is. This is because we are motivated by the gap between what should be and what is. We see these gaps between our rational expectations of how an animal should behave according to the theory of natural selection, and a seemingly irrational reality of how it’s actually behaving, and we then try to find rational explanations for that gap. But whether or not something appears rational or irrational depends extremely strongly on our assumptions!

The impact of our assumptions on the nature of inquiry in evolutionary biology is quite clear in a question we tackled in a collaborative paper coauthored by Julia Monk, Erin Giglio, me, Max Lambert and Caitlin McDonough. What we take on in this paper is the way we currently study same sex sexual behavior which we call SSB and its evolutionary relationship with different sex sexual behavior, which we call DSB. Specifically, we ask, what are the assumptions that lead SSB to be considered a paradox?

I’m going to start by describing how SSB is currently considered a paradox. In sexually reproducing animals, by and large, mating with individuals of the same sex is not going to produce offspring, and thus does not immediately contribute to fitness. And so it seems paradoxical for animals to expend time and energy in mating with individuals of the same sex, because that’s time and energy that they are not spending on producing offspring by engaging in DSB, and so we expect natural selection would act against SSB if it were to arise in a population because natural selection maximizes fitness. However, SSB persists, so there must be either an explanation for why it persists that relies either on some other benefits that haven’t yet been considered, or on some constraints that prevent fitness maximization from being realized.

And what we do in our paper is to upturn this narrative by asking a couple of simple questions about the assumptions underlying it. First is the assumption that engaging in SSB is costly to fitness, that individuals that engage in SSB have lower fitness—but what if it’s not? What if, in general, SSB is one of many, many, many reasons that a mating may not lead to the production of offspring? Second, there is an assumption that SSB has evolved from an ancestral state of DSB, but what if that’s not true, and the ancestral state is, instead, mating behavior that is indiscriminate with regard to sex? It’s worth noting that both of the assumptions we question here are aligned with a social and political status quo of heteronormativity at best and homophobia at worst, on the heteronormative notions of queer sex as aberrational and somehow excessive.

 In our paper, we conjecture that in fact across animals, SSB is not all that costly in terms of time, energy, and fitness, and this would imply that when we look carefully and unbiasedly, we will see tons of variation across individuals and populations in the degree of SSB, in a manner that is influenced by context dependent costs and benefits, historical contingencies, and more. And further we expect this variation to manifest across the animal phylogeny, tracing back to an ancestor that mates indiscriminately.

Our paper was one in which we posed alternative hypotheses and new questions to consider empirically, and it was really exciting to see that our paper has already motivated further research that builds on our ideas, formalizes them mathematically, and shows that they are quite plausible. 

Okay, so now we’re going to move to asking about the political underpinnings of a narrative of adaptationism. This link becomes really clear when we ask, where does the normativity of adaptationism come from? Why are we focused on these notions of what “should be” happening?

The clearest explanation comes from philosopher Samir Okasha’s work on agents and goals in evolution, where he clearly traces this normativity to the notion of the rational agent. Okasha draws the parallels between adaptationism and rationality when he says, “In both cases we begin with a conception of how things should be in order that a particular end be achieved, and try to show that how they actually are is a close match.” And the part I want to highlight here is the “in order that a particular end be achieved”—that end is not “is this the best explanation for the data?”, the end is “how can we think of these data as being consistent with the framework centered on fitness maximization?”

Moreover, this rational agent underlies both how we think about adaptation and how we think about human interactions in a capitalist economy. And this is reflected not just in the way we talk about maximization, of fitness or of utility, but also in the mathematical tools of game theory that we employ in both domains as a further formalization of the actions of the rational agent.

So what are some other ways of looking at the world, that don’t privilege adaptation above all else? If we come back to the notion of standpoint theory, we can ask—who has engaged in political struggle against capitalism, and how do they look at the world?

One compelling option is the dialectical materialist lens where instead of a construction based on what should be and what is, we ask “what is, what could have led to it, and what happens now that we are here?” And we lose that outsized focus on normativity, and adaptation becomes one of many processes that are interconnected and contingent on one another.  And while it’s difficult for me to say exactly what distortions the dialectical materialist lens is going to produce, I can say that the focus here is not so much on any one process, but on the mechanistic and historically contingent connections between them.

And so I want to end by telling you about an organism that, more than any other animal I’ve encountered, insists upon this different way of thinking, and that is the tent caterpillar. At the start of my time in the Miller, I was in search of a new study system where I could study social interactions in the context of group living animals that build nests, and tent caterpillars seemed like an awesome group in which to work because we know a ton about their basic biology and natural history. But we’ve known about their natural history for quite a while, and yet they don’t seem to show up as an organism that are used to understand broader conceptual things about the evolution of behavior, collective behavior, social behavior and so on. And James Costa, a phenomenal scholar of the “other insect societies”, which is to say not bees or wasps or ants or termites, has made this same lament, that it is weird that we don’t better understand tent caterpillar sociality in the broader conceptual context of behavioral ecology. And so my initial thought was that I would be able to read about them and watch them and come up with the right adaptive questions to start asking.  

But my contention now is that the adaptationist lens is the wrong lens for tent caterpillars—it distorts or renders opaque more than it clarifies. Basically, I think that tent caterpillars are conceptually inaccessible, not uniquely but more so than many other organisms that we study, from an adaptationist perspective. And this became apparent to me when I read the Dialectical Biologist by Richard Levins and Richard Lewontin. This book not only helped me understand why tent caterpillars are a thorn in the side of adaptationism but also offers a way forward.

And so the starting point here is different, it’s this contention that in any system, what constitutes the parts is defined by the whole of the system, that you simply can’t break things down. And so this means, specifically, that when you are dealing with organisms that interact with one another and with their environment, which is every organism, you have to think about two things. First, you have to think about how various levels of organization, so from gene to individual to populations to communities and species, are only partly autonomous and reciprocally interacting and so in the context of selection you need a multilevel selection approach that group selection. And this is extremely clear in the case of tent caterpillars where, first of all, there are a ton of them and they forage together and shelter together and clearly impact one another’s life, but second, these groups are in fact very fluid and not necessarily made up of relatives later in the season and they become more solitary as they age, suggesting that you can’t simply treat groups as fixed units (as you can with bees and ants and termites, often), but also you can’t ignore the groups—they are partly autonomous and reciprocally interacting.

And second, our dialectical materialist approach that contends that parts and wholes cannot be separated implies that you have to think about organisms and environments actively codetermining each other, in the way that is suggested by niche construction discourse. And here again, tent caterpillars are a great exemplar. Not only do they literally construct this tent-like structure in which they shelter and on which they interact and communicate with one another, but also their main activity in this time of their life is eating leaves, and by eating the leaves that surround them, they are directly changing the environmental conditions of their surroundings, and these conditions in turn determine their growth, their hunger, and their further capacity to shape their environments—the organism and the environment are codetermining one another.

So tent caterpillars are, to me, making the case for a different way of looking at nature than currently offered by the adaptationist lens that shapes my field of behavioral ecology, and I think we will learn something new about them from a dialectical materialist approach that is grounded in multilevel selection and niche construction. But I don’t think it’s just tent caterpillars. I think we’ll learn more about every organism from this dialectical materialist perspective, because every organism interacts with other organisms and with its environment. And I think this is where the dialectical future of behavioral ecology lies.

So it is possible to think differently that we currently do, and more importantly, is it possible to actually do things differently? And the answer is clearly yes. Because we need to, we need to imagine different questions, with more nuance, consistently interrogating assumptions if we want to do a better job of understanding and engaging with nature. And to do this effectively, we have to embrace our politics explicitly, not only because we can never escape our politics but because our politics are epistemologically informative.

I want to end by emphasizing that almost none of the overarching critique of adaptationism I’ve described to you here is new, these have been well constructed within biology in the work of evolutionary biologists such as Stephen J. Gould, Richard Lewontin, Richard Levins, David Sloan Wilson, Kevin Laland, Eva Jablonka, Marion Lamb, and more. These critiques are also well developed in fields of scholarship outside of biology, in fields such as science and technology studies, philosophy, and the history of science. What we need now isn’t just more critique, what we need is actionable change from scientists in the ways in which we construct our questions and how we are explicit about their political underpinnings.

I’ve been trying to do this in my own work, such as in a recent paper on character displacement, in an ecosystem of these two interacting lizards found on these small islands of the east coast of Florida that we first sampled in 2010 and then went back to in 2019. Our goal was initially to show that the very adaptive process of character displacement is important despite variation across space and time, and we presented our findings that way. But I read the dialectical biologist between our initial submission of this paper and the revised submission, and I realized the underlying adaptationism in our paper, and in the revisions we were able to re-approach these data with much less of a focus on the adaptive process and much more from the perspective that the messy realities of both inexplicable variation across space and time and doing opportunistically longterm fieldwork were not in opposition to the story of character displacement but in fact makes it way more interesting. And here’s a really tangible example of a change we made. In our initial submission, we had these data from 2019 in the main paper—the details don’t matter, but you can see how nice and parallel all these lines are. The much messier 2010 data were initially in the supplementary material—we weren’t ignoring them, but they didn’t fit the adaptive narrative we had fit our results into. But in the final paper, we included them both in the main paper, along with hypothesized non-adaptive reasons for the differences we saw between 2010 and 2019.

And stepping back, a broader effort I’m especially excited about is a recent call for papers to be published in a scientific journal, read by scientists, for which we’ve assembled a team of editors who work in disciplines across the natural and social sciences and humanities, and our goal is specifically to bring  interdisciplinary critique of the scientific process in front of the eyes of scientists but also for authors to make concrete suggestions for how scientific practice can change when we consider diverse standpoints. And so while I know that all of you here deeply believe in the value of interdisciplinarity within the natural and physical sciences, I’d urge you to consider extending this umbrella to the social sciences and humanities as well, because you may be surprised by the impact this will have on your own scientific research.

With that, I just want to acknowledge all the people who’ve influenced this talk, including my coaches, thanks to everyone in the Miller community and thanks to you all for listening.