The Macroevolutionary Puzzle of the Cycads

Derek Turner writes . . .

Living Fossils

Cycads, along with coelacanths, horseshoe crabs, and chambered nautiluses, are important examples of “living fossils.” (I wrote a bit about living fossils in my last post as well.) Most people give credit to Charles Darwin for coining that term in the Origin of Species, though it also has quite a strange prehistory that goes back well before Darwin, to stories that miners used to tell about discovering living (presumably antediluvian) toads and other creatures hibernating in solid rock.

Today, however, many scientists are somewhat ambivalent about the notion of a living fossil. (And some are downright hostile.) Part of the problem is that the status of some of the classic cases of living fossils—including cycads—is murky. (For an interesting defense of the notion of a "living fossil," as well as a helpful discussion of cycad biology, see this blog essay by Jennifer Frazer.) 

I took this picture of a cycad in Port Elizabeth, South Africa, while traveling there with colleagues in 2013.

I took this picture of a cycad in Port Elizabeth, South Africa, while traveling there with colleagues in 2013.

Cycads do seem to present us with an interesting case of morphological stasis. Not long ago, a team of Chinese paleontologists reported the discovery of a remarkable cycad megafossil.[1] If you look at an image of the cycad megafossil, it is very hard to distinguish it from a run-of-the mill sago palm (also a cycad) that many people like to keep as a houseplant. (You can read the paper and check out the image here.)  Pretty much anyone can keep a houseplant that is a lot like the plants that the dinosaurs liked to munch on.

Indeed, one possibility is that the extinction of the dinosaurs that they coevolved with helps explain the post-Mesozoic decline of cycad biodiversity. Competition from flowering plants may also part of the story.

Fossil cycads from N. America, courtesy of Wikimedia commons.

Fossil cycads from N. America, courtesy of Wikimedia commons.

A Recent Radiation                                                              

But it’s not totally obvious that cycads deserve to be considered living fossils, either. One difference between cycads and other living fossils is that there are still quite a lot of cycad species hanging around—about 300 species belonging to 6 genera, even though their diversity was much greater during the Mesozoic. Contrast that with, say, the coelacanth (2 species), or the wollemi pine (just 1 species), New Zealand’s tuataras (1 species), or nautiluses (6 species).

Not only that, but when scientists recently did a molecular clock study on a large sample of extant cycad species, they found that most of those species were not actually very old! [2] 

Molecular clock studies use comparisons of DNA and/or protein structure across species, together with assumptions about the rate at which changes in those chemical structures accumulate, to draw conclusions about how far back in the past the species shared a common ancestor. In the case of the cycads, the scientists found that there was a big burst of speciation—a major radiation—only about 12 million years ago, during the late Miocene. Most of the living species of cycads have common ancestors that lived around that time. This recent burst of evolutionary activity doesn’t fit too well with the idea of living fossils as the last remnants of a group whose evolutionary glory days lie far back in the mists of deep time. Instead, the cycads have been making a more recent evolutionary comeback.  

It turns out that cycads are not the only putative living fossils whose status has been challenged. Other scientists have raised doubts about coelacanths, too, though on different grounds. [3] One might wonder whether paleontology and evolutionary biology even need the concept of a living fossil. What sort of work does that concept do?


Distinct Evolutionary Phenomena

Part of the confusion, perhaps, is that “living fossil” is often used to cover a variety of different evolutionary phenomena, but those phenomena do not always co-occur.

(1)  Species longevity. Sometimes a particular species can hang on for a really long time. (See our earlier discussion of expiration dates and species lifespans.)

(2)  Long-term morphological stability. Sometimes particular traits or structures persist for a very long time in the fossil record without much change. Of course, whether you “see” stability depends on which trait you’re looking at, on the grain at which you describe the traits, and so on.

(3)  Persistence in the wake of severe of biodiversity reduction and/or loss of abundance. In some cases, there are groups that were abundant and diverse in the deep past. Some members of the group could hang on for a long time with very low abundance, even after most of their biodiversity has been lost.

When we talk about “living fossils,” we should be precise about which of these phenomena we have in mind. Cycads seem to afford a great example of (2) long-term morphological stability. But they are not such a good example of (3), given their relatively recent radiation. On the other hand, coelacanths (for example) are better examples of (3) persistence in the wake of biodiversity loss, though their degree of morphological stability is up for discussion.


Habitat Tracking?

Importantly, these three distinct phenomena might call for different sorts of evolutionary explanations. To make this a little more concrete, habitat tracking is one mechanism that scientists sometimes invoke to explain morphological stasis. When environmental conditions change, some populations that can do so simply follow their preferred habitat, rather than adapting to the new conditions. Habitat tracking could be an important part of the story about morphological stasis in some living fossil cases, and it could even help explain why some particular species persist for a long time, but it’s a little harder to to see how that could explain stasis in the cycad case, given what we know about their recent radiation and large geographic range. Habitat tracking might work best as an explanation where (2) stasis co-occurs with either (1) or (3).

 Cycads exhibit a lot of morphological stability (though their recent radiation surely did not occur without some evolutionary change). But one of the classic explanations of stability (habitat tracking) is off the table in this case, because it doesn’t fit well with what we now know about the cycads’ recent evolutionary radiation.


A Macroevolutionary Puzzle

The story of the cycads seems to be one of decline (both in abundance and in diversity), persistence, and resurgence around 12 million years ago. This sort of pattern poses a peculiar explanatory challenge. Whatever factors initially caused the cycads to go into decline (the loss of their dinosaurian evolutionary partners, increased competition from flowering plants, etc.) were probably still in place 12 million years ago. So what exactly happened during the late Miocene to give the cycads their second wind, so to speak?

Nagalingum and colleagues point to some late Miocene paleogeographic and climate trends as possible triggers. Seaways between North and South America, and between Africa and Eurasia, were closed as the continents assumed their current positions. And the planet was getting somewhat cooler. Could these events have set the stage for a cycad comeback? (How, exactly?) Or might their comeback have had something to do with the weevils that pollinate many cycad species today?

Even if we could explain the cycad radiation, we might also want to know why it was not accompanied by more significant morphological change. Niles Eldredge and Stephen Jay Gould’s punctuated equilibria model suggests that morphological change happens rapidly during speciation episodes. But the cycads seem to have experienced a lot of speciation without much drastic morphological change. So what was going on, exactly?

I hope that this post leaves you scratching your head a little bit. If you have ideas, or if you know something about cycads that I don't, please do share below.

The fact that cycads are so puzzling, from an evolutionary perspective, makes it even sadder that Fossil Cycad National Monument no longer exists. Hopefully we can do a better job protecting the living cycad species than we did protecting the fossils!


[1] Wang, X., Nan, L., Wang, Y., and Zheng, S. (2009), “The discovery of whole-plant fossil cycad from the upper Triassic in western Liaoning and its significance,” Chinese Science Bulletin S4: 3116-3119. 

[2] Nagalingum, et al. (2011), “Recent Synhronous Radiation of a Living Fossil,” Science 334: 796-799.

[3] Casane, D., and P. Laurenti (2013), “Why coelacanths are not ‘living fossils’,” Bioessays 35: 332-338

Extinction and Expiration Dates

A Conversation with Joyce Havstad about Species Selection

A coelacanth at the Naturhistorisches Museum in Vienna. Some species just seem to go on and on . . . and on and on. They don't have expiration dates. Is this a problem for the theory of species selection?

A coelacanth at the Naturhistorisches Museum in Vienna. Some species just seem to go on and on . . . and on and on. They don't have expiration dates. Is this a problem for the theory of species selection?

Derek Turner writes ...

Joyce Havstad offers an incredibly careful and generous discussion of my Paleontology book. (Hi Joyce – and thanks!) Every philosopher should be lucky enough to get such careful and challenging feedback. Joyce makes some critical points and raises some questions about important technical details. Here I want to pick up on just one of the challenges that she raises. In the book I am pretty sympathetic toward the theory of species selection. Joyce, however, highlights a really interesting problem for that theory, one that I don’t consider in the book at all. Nor do I know of anyone else who discusses it. (Readers, if you know of any scientists or philosophers who have thought about this, can you please share?) It seems like this problem, which I’ll call the Expiration Date Problem, needs some attention.


What is Species Selection all About?

When Darwin formulated the theory of natural selection, he was thinking about the differential survival and reproduction of individuals within a population. But what if whole species are going through a similar process at a higher level? Differential speciation and extinction seem a lot like differential reproduction and survival.

Steven Stanley, a paleontologist, described species selection in a paper he published in 1975:

In this higher-level process species become analogous to individuals, and speciation replaces reproduction. The random aspects of speciation take the place of mutation. Whereas, natural selection operates upon individuals within populations, species selection operates upon species within higher taxa, determining statistical trends. In natural selection types of individuals are favored that tend to (A) survive to reproduction age and (B) exhibit high fecundity. The two comparable traits of species selection are (A) survival for long periods, which increases the chance of speciation, and (B) the tendency to speciate at high rates. Extinction, of course, replaces death in the analogy (p. 648).[1]

Notice how Stanley draws a parallel between the following two phenomena:

(A)  An organism surviving to reproductive age.

(A*) A whole species surviving for a long period, “which increases the chance of speciation”

Joyce’s worry—the problem of expiration dates—is that there is a relevant difference between organisms and species that may cause trouble for Stanley’s analogy here.


The Problem of Expiration Dates

Joyce writes:

By far the majority of organisms have an unyielding expiration date.  There’s an upper bound on how long they can live before they die.  Organismal fitness is therefore constituted by both survival and reproduction, but the former is mostly important as a way of guaranteeing the latter.  Species, however, can perdure—and therefore, survival can be a more independent and significant contributor to fitness.”

This is a really good point. Ordinary organisms have a maximum lifespan. But species can, at least in principle, last indefinitely. Species have no “unyielding expiration date,” as Joyce aptly puts it. Perhaps some “living fossil” species are good examples of this—think of horseshoe crabs or the coelacanth pictured above. Some species do seem to persist for many millions of years, with no clear upper bound on how long they may last. The question is whether this difference matters, and if so, how.

Joyce argues that this difference between species and individual organisms might affect how we think about some of the famous alleged cases of species selection, such as Elisabeth Vrba’s case of the African antelopes.

Vrba compared impalas with wildebeests over the last several million years.[2] Although impalas are more abundant (in the sense that there are more individual animals), wildebeests are a more species-rich group. In the last five or six million years, impalas have barely speciated at all, whereas there are many more species of wildebeests. This looks like an interesting case where species-level fitness and organism-level fitness pull apart. And on more liberal conceptions of species selection, that pulling apart is what you really need. Their abundance suggests that individual impalas are doing pretty well in their environment, but the low speciation rate suggests a lower species-level fitness. 

(One qualification: Vrba herself did not really think of this case as a case of species selection. She called it “effect macroevolution,” because she thought that the differential speciation rates of impalas vs. wildebeests were just a side effect of ordinary microevolutionary processes. But some people who take a more liberal view of what counts as species selection might consider this to be a good example of it.)

Joyce raises an important conceptual question: Is it really correct to say that the impalas have a lower species-level fitness? We need to be careful to avoid thinking of species-level fitness as nothing more than speciation propensity. Persistence (the species-level analogue of survival) matters too! And this is where the disanalogy mentioned above starts to become an issue. If the impala species had an upper bound on how long they could last—if they were really like individual organisms—then the low speciation rate really would make for lower species-level fitness. But of course with whole species, there’s no upper bound. The impalas might have a much lower extinction risk than the wildebeest species do. In fact this is really plausible. Part of Vrba’s original argument was that the impalas are ecological generalists, while the wildebeest species tend to specialize more on particular food sources. In general, generalists have lower extinction risk. So taking Joyce’s point into account, it could be that Vrba’s (and my) initial take on this case is not quite right: Maybe the impalas are not less fit at the species level than the wildebeests at all!


Why do we need the theory of species selection?

Species-level fitness has two ingredients: speciation propensity and extinction risk. How do those fit together, in Vrba’s case, and others? The lack of expiration dates makes this question tough to answer.

Now here is a philosophical trial balloon: One possible response to this problem might be to stop worrying about estimating species level fitness. Instead, perhaps, the right approach is to try to estimate speciation propensity and extinction risk independently, treating those as two different factors that can make a difference to macroevolutionary patterns. Perhaps one could concede the difficulty of saying exactly how to combine these into a single quantity (species-level fitness), while arguing that treating them independently still gets us most of what we could reasonably want from the theory of species selection.

This response requires us to say a bit about what the theory of species selection is for. Here I think the theory might have payoff in two different domains:

(1)   Species selection gives us one possible way of explaining certain large-scale patterns and trends in evolutionary history.

(2)   Species selection also gives us a useful (possibly predictive) perspective on the current biodiversity crisis, because we are now in a period of artificial species selection, where human activities are biasing macroevolutionary processes.

The second point is especially important, though it remains under-explored. In an important 2008 review paper, David Jablonski wrote that “[t]oday’s biota appears to be in the midst of a massive experiment in strict-sense species selection” (p. 515).[3] If Jablonski is right, species selection theory could be another paleontological contribution to conservation biology.

It might be possible to make good on both projects (1) and (2) without really solving the problem of expiration dates. For example, it might be possible to generate interesting explanations of large-scale evolutionary patterns merely by estimating differential extinction risk. If burrowing animals have a lower extinction risk when a meteoroid hits, that alone can help explain resulting patterns in the fossil record. And for that explanatory purpose, it might not matter much how extinction risk combines with speciation propensity to constitute species-level fitness. Similarly, with respect to project (2), it could be really useful to estimate extinction risks of different species, even without worrying so much about how the extinction risk goes together with speciation propensity to constitute species-level fitness.

In other words—and this is just a trial balloon—maybe the ingredients of species-level fitness are more interesting and important than speciesl-level fitness itself.


[1] Stanley, S. (1975), “A Theory of Evolution Above the Species Level,” Proceedings of the National Academy of Sciences 72(2): 6467-650.

[2] Vrba, E. (1987), “Ecology in relation to speciation rates: Some case histories of Miocene-Recent mammal clades,” Evolutionary Ecology 1: 283-300.

[3] Jablonski, D. (2008), “Species Selection: Theory and Data,” Annual Review of Ecology, Evolution, and Systematics 39: 501-524.