Life cycles in major transitions, and some clueless critique

Jordi van Gestel and Corina Tarnita have published a ‘Perspective’ in PNAS, “On the origin of biological construction, with a focus on multicellularity“:

…we propose an integrative bottom-up approach for studying the dynamics underlying hierarchical evolutionary transitions, which builds on and synthesizes existing knowledge. This approach highlights the crucial role of the ecology and development of the solitary ancestor in the emergence and subsequent evolution of groups, and it stresses the paramount importance of the life cycle: only by evaluating groups in the context of their life cycle can we unravel the evolutionary trajectory of hierarchical transitions.

van Gestel 2017 Fig. 2

Figure 2 from van Gestel and Tarnita, 2017. Relationship between life stages in hypothesized life cycles of solitary ancestors and group formation in derived group life cycles. (Upper) Simplified depiction of hypothesized ancestral solitary life cycles of the green alga Volvox carteri, the cellular slime mold Dictyostelium discoideum, and the wasp Polistes metricus. Life cycles here consist of a life stage expressed under good conditions (black) and a life stage expressed under adverse conditions (green). For the latter life stage, we show an environmental signal that might trigger it and some phenotypic consequences. (Lower) Simplified depiction of group life cycles of: V. carteri, D. discoideum, and P. metricus. Developmental program underlying life stages in solitary ancestor is co-opted for group formation (shown in green): differentiation of somatic cells (V. carteri), fruiting body formation (D. discoideum), and appearance of foundress phenotype (P. metricus).

The article is essentially an essay arguing that an understanding of the Major Transitions (which they call ‘hierarchical evolutionary transitions’ or HET; more on that below) is going to require both a top-down and a bottom-up approach. They define the top-down approach as one that starts with

…paradigmatic examples of biological units, identifies their properties (e.g., high level of cooperation, reduced conflict, differentiated types, metabolic specialization), and explores how a group could have evolved each of these properties.

This approach, they argue, is limited:

While [the top-down] approach has revealed a wealth of valuable insights, we argue that it is insufficient to understand the origin and evolution of HET.

This type of top-down approach to the study of HET runs into two critical problems. First, by focusing on properties of groups that qualify as paradigmatic examples of biological units, studies largely ignore the ancestor, including its internal organization and properties, the ecological context, and the mechanisms that gave rise to the primitive instantiations of those groups.

I don’t really agree that top-down approaches ‘ignore the ancestor’; much comparative work, including my own PhD research, is focused precisely on understanding the nature of the unicellular ancestors of modern multicellular groups. It’s true, though, that our relative ignorance of these ancestors is an important limitation. We often use extant unicellular relatives as stand-ins for ancestors, and this, as I’ve argued before, is an approximation at best.

Second, in addition to ignoring the ancestral properties, by fixating on certain properties common to the known paradigmatic examples of HET, the top-down approach fails to explore the full potential of evolutionary trajectories and transitions, not only the paradigmatic but also the peripheral, and not only the actual (i.e., realized) but also the possible.

This is, I think, a fair critique. There have been a few theoretical papers that have attempted to visualize ‘not only the actual (i.e., realized) but also the possible’ routes to multicellularity, but the range of outcomes we can envision is likely to be more limited than the possible range. I think about this sometimes, in the context of astrobiology. If we lived on a world without eusocial animals, would we ever conceive of them? Would we ever wonder ‘why don’t animals ever form societies of tens of thousands of individuals where only one gets to reproduce and the others specialize into several functionally and morphologically differentiated, sterile castes’? If we didn’t know about the endosymbiotic events that led to mitochondria and chloroplasts, would we ever conceive that a cell could take up residence within another cell and evolve into an organelle? For that matter, if we lived in a strictly unicellular world, would we ever wonder why a few trillion of us had never stuck together and specialized into a hundred or so cell types to form one giant, integrated individual? I doubt it. The outcomes of evolution are, I think, stranger than anything we could have conceived if we didn’t observe them; the paths not taken are likely more numerous than we can imagine.

So I completely agree that the top-down approach has limitations. That’s largely what motivates my lab‘s microbial evolution experiments with Chlamydomonas and, I dare say, Will Ratcliff‘s experiments with yeast. To overcome these limitations, van Gestel and Tarnita propose

…a bottom-up approach to study the dynamics underlying HET, which builds on and integrates knowledge from existing research programs on biological construction: phylogenetic, empirical (e.g., experimental evolution, developmental biology, sociobiology), and theoretical (e.g., on multilevel-selection, cooperation, self-organization).

with which they propose to address a set of questions relevant to these transitions:

Q1: When/how does a group originate that has the potential to undergo a HET?

Q2: What emergent properties do these groups have?

Q3: How does selection act on these properties?

Q4: How does this affect the ancestral developmental program(s) and change group properties?

Q5: When/how does this lead to novel organizing/developmental principles within the new unit?

Q6: What kinds of organizing complexity can evolve?

They go on to consider each of these questions in turn and conclude

We argue that only by starting with the solitary ancestor and its life cycle, and studying these six questions, can we derive an understanding of the causal factors underlying HET. Then, by comparing different instantiations of the same transition (e.g., the multiple origins and transitions to multicellularity), we can determine whether the same causal factors underlie different transitions and which causal factors explain the different organizational outcomes of those transitions.

I think this is all pretty non-controversial. Sure, others would come up with different lists of questions, but of course these are all things we want to know. Van Gestel and Tarnita are essentially proposing a research program here, one to which they’ve already made some contributions. Who could have a problem with that?

The same people who have a problem with anything to do with the evolution of multicellularity. Predictably, the Discovery Institute has some clueless critique (“Bottom-Up Bottoms Out“). Unfortunately, it’s hard to say exactly who has the problem, since the article is only signed by “Evolution News“.

In any other scientific arena, the amount of failure we’re about to see would send scientists out the door of the science building in disgrace to look for a new job. When it comes to evolutionary biology, however — since no alternatives are allowed — the advocates of scientific materialism are allowed to completely ignore logical alternatives and to fail with impunity, even after well over a century of trying.

Wow, that’s harsh! I’m sure we’re going to see some rock-solid criticism to back that up.

Let’s introduce Jordi van Gestel and Corina E. Tarnita. Their paper in the Proceedings of the National Academy of Sciences, “On the origin of biological construction, with a focus on multicellularity,” is made to order for a debate. But don’t hold your breath. These evolutionists from the University of Zurich and from Princeton, respectively, address the topic, “Resolved: Bottom-up approaches are superior to top-down approaches for explaining the origin of hierarchical biological organization.”

Well, no. That’s not what the paper says. What it says is that top-down approaches alone can’t tell us everything we need to know about the Major Transitions, and that they need to be combined with a bottom-up approach:

…in this Perspective we propose a bottom-up approach to study the dynamics underlying HET, which builds on and integrates knowledge from existing research programs on biological construction: phylogenetic, empirical (e.g., experimental evolution, developmental biology, sociobiology), and theoretical (e.g., on multilevel-selection, cooperation, self-organization).

The word “superior” doesn’t appear in the paper. So our anonymous author has set up a straw man argument right out of the gate. I wouldn’t want my name on that, either. The critique quotes the van Gestel and Tarnita paper:

Despite considerable advances, there is no bottom-up, dynamical account of how, starting from the solitary ancestor, the first groups originate and subsequently evolve the organizing principles that qualify them as new units.

and comments

This admission of failure is not a good way to end a scientific paper, so they try something new.

Yes, that’s right. The fact that we don’t already know everything about the evolution of multicellularity is a massive fail, and van Gestel and Tarnita should be sent ‘out the door of the science building’ for trying to learn more:

Everything evolutionists have tried before is a failure, but take heart: we have a new series of questions, they basically say.

Yeah, that’s not what they said. If you had good arguments, you wouldn’t need to misrepresent theirs.

It will sound more scientific to throw in some recondite jargon. They announce a new made-up acronym, “HET” for “hierarchical evolutionary transition.”

If anyone knows the value of sounding sciencey, it’s the Discovery Institute. Look, we use abbreviations and acronyms in scientific papers to save space. When a phrase gets repeated over and over again throughout a paper, it makes sense to shorten it. Sort of like intelligent design advocates do with ‘complex specified information’ (CSI) and ‘chloroquine complexity cluster’ (CCC). What exactly is the problem with that?

Presumably, this includes the Cambrian explosion, though they don’t mention it.

No, it doesn’t. Nooooo. Van Gestel and Tarnita define HETs as events in which

…simple units assembled into groups that themselves became new units of biological organization.

This is similar to, but more restricted than, Maynard Smith and Szathmáry’s “Major Transitions in Evolution” and Michod’s “Evolutionary Transitions in Individuality”. Here’s Maynard Smith and Szathmáry’s list of the Major Transitions:

Table 1.2 from Maynard Smith J, Szathmáry E (1995) The Major Transitions in Evolution. Oxford University Press, Oxford.

Do you see the Cambrian explosion there? You won’t see it in Michod’s list either, or in Szathmáry’s “Major Transitions 2.0”, or O’Malley & Powell’s. No one thinks that the Cambrian explosion involves “simple units assembl[ing] into groups that themselves became new units of biological organization.” The origin of animal multicellularity must have happened before the Cambrian explosion, probably long before.

Since van Gestel and Tarnita are so clear about what they mean by hierarchical evolutionary transitions, saying that they ‘presumably’ mean something completely different is some pretty egregious intellectual dishonesty.

It goes on in that vein for a while: contemptuous dismissal of material the author either doesn’t understand or is willfully misinterpreting, all premised on the assumption that anything we don’t yet know about the evolution of multicellularity is a failure of science. Yes, van Gestel and Tarnita point out that we don’t know everything about the evolution of multicellularity, and they are absolutely right. The fact that we don’t know everything is not an indictment of science; it is the reason we do science.


Stable links:

Gestel, J. van, and C. E. Tarnita. 2017. On the origin of biological construction, with a focus on multicellularity. Proceedings of the National Academy of Sciences, USA, Early edition. doi: 10.1073/pnas.1704631114



  1. jazzlet says

    Urgh, what a load of slug slime. It makes me feel dirty just reading the bits you quoted from Evolution News. No wonder they don’t want to put their name to the article.

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