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Functional adaptations: ontogeny and evolution

As I study functional morphology for my thesis, I think about this subject an unusual (or unhealthy) amount. And there's one thing that's been hurting my head for the last few days.

That is: how does physical stress as a response to function, e.g. biting reaction force and its skeletal response, work as selective pressure on morphology? In other words, what are the mechanisms behind functional adaptation as seen by morphological change through time?

Skeletal response to mechanical stresses occur during the lifetime of an individual. These are ontogenetic developments that are not the same as primary ontogenetic development, as shared by all members of the species (predestined by the genome), but secondary responses brought about by extrinsic factors. So surely, any changes acquired as a direct response to extrinsic mechanical stresses, must be acquired traits, thus aren't passed down to the next generation.

My question therefore is, how do these acquired traits get passed down to the descendants? We could trace functional adaptations through the evolutionary history of certain animals, e.g. the increasing robusticity in tyrannosaur skulls. Thus, it is quite possible that skeletal response to extrinsic forces, whether it be to withstand higher biting stresses or increased muscle forces, are effectively being passed down. Otherwise, taking structural stresses and strains of an animal and linking it in with evolution is completely pointless - we can see how extrinsic stresses affect ontogeny but not evolution.

Or is it that, every single member of derived tyrannosaurids go through this ontogenetic change independently within their individual lifetimes as a response to certain extrinsic pressures and consequently ending up with the same adult morphology? So in other words, is it that Tyrannosaurus wasn't genetically predestined to have more robust skull morphology than Daspletosaurus but rather led significantly more rough lifestyles? This basically means that responses to extrinsic factors are not passed down but acquired separately in every generation, and independently in every single individual within their respective lifetimes.

Or perhaps, the more responsive individuals fare better and naturally get selected for, thus increasing the mean response level in the population, eventually producing a descendant population with significantly higher responses to the same extrinsic stresses than the ancestral population. So, perhaps it is this responsiveness that are hereditary? In the case with tyrannosaurs, Tyrannosaurus possibly may have had higher response levels to extrinsic forces than Daspletosaurus which led to increased skull robusticity during ontogeny.

Or, from basic theory of evolution, is there a background variation in predestined skull robustness that some just so happens to perform better under extrinsic forces than others in a typical tyrannosaur lifestyle and that they are naturally selected for, and given enough time the population mean skull robustness shifts towards increased robustness in derived tyrannosaurs, most notably in Tyrannosaurus? In this case, skeletal response to extrinsic factors are not passed down but those that perform better to those factors are selected for from a population with varied degrees of responses.


I don't know the answer. I wonder if anyone has an answer...

Comments

Neil said…
Wow, you raise some really interesting points here that touch on a lot of outstanding issues in paleontology (Cope's "rule", ecophenotypic variation and the morphological species concept, etc.).

I'm not about to claim I have an answer, but it seems like you could test at least some of these options, though it might be rather difficult in fossil taxa with relatively few specimens.

Clearly there is some hereditary basis to 'absolute' morphology and morphological response to environmental conditions so I think your final two options are probably both in play to some degree.

Untangling them in an extinct organism seems pretty difficult however...the best experimental investigation I can imagine would be looking at the range of variability vs. absolute morphology in living animals.

One way to do this (kinda ghoulish and I'm not really suggesting it) would be to compare calves raised in a veal crate vs. free range (or perhaps just under different excercise regimens) and see the over all range of ecophenotypic variablity, then do the same thing with other bovids of different size (sheep, goats etc.) This would help you to see if larger taxa show an increase in environmental responsiveness as well as just absolute morphology...It's not going to tell you much about tyrannosaurs of course....

Plus, you'll probably have to through in sexual selection as a possible factor and one that might have complex interactions with both environmental stress and overall morphological variability within a population.

The Tyrannosaurus/Daspletosaurus ecotype option you raise is more troubling, especially for those of us who depend heavily on the morphological species concept. Luckily, animals don't seem to be quite as plastic as plants in this regard.

The only way I can really imagine getting at this question in two very closely related fossil taxa, try to quantify all of their morphological variability and then see if you can realistically ascribe that variability to environmental influence, with special attention paid to characters unlikely to be environmentally contingent (like tooth count say). Of course at the end of the day I think paleontologists have to accept that "morphospecies" are imperfect constructs (I would argue that "biospecies" have their own issues as well).

Speaking of headaches for the functional morphologist...did you see the Cuozzo and Sauther talk at SVP? They discussed a whole population of lemurs feeding outside the functional limits of their dentition and shattering the hell out of their teeth. Supposedly this was a response to the extinction of large-bodied lemurs which had previously filled the "hard nut" niche.

It made me wonder if the important question in functional morphology might not be what can taxon X do with trait Y but, what can't taxon X do with trait Y that it might want to...and would be willing to make a fast sprint across a hostile adaptive landscape in order to get there (hard core anthropomorphizing there, but you get the point).
Wow, thanks for your insights!

I agree that comparing two populations of domestic animals raised in different environments will probably be a good way to test this. Maybe even have them fed on food of different toughness. I guess you can do this with lab rats or mice and feed them food of different toughness for several generations, trace morphological change through ontogeny within each generation and any differences across generations, then compare these observations in your different groups...

...though as you mention with sexual selection, it'll probably be another headache to try and determine which morphological differences, if any between generations or populations, can correctly be assigned to environmental/ecological/functional influences.

And I'd missed that talk as SVP. Sounds really interesting.

I also agree on your final point about functional morphology and answering what can't animals do - kind of like John Hutchinson's attitude towards locomotion in T. rex - we won't know how T. rex may have walked but we do know T. rex definitely did not walk this way.
I think it's a fitness issue.. a mesozoic predator facing some pretty challenging mouthfulls would have probably picked up several bad injuries in it's life time. Naturally any variations in bite performance popping up within a population would have a big opportunity to get established if they reduced the likelihood of tooth ache. It looks like the important factor is that variation allowing increased fitness goes on to be sealed within the population's and then the species' genome. The behaviour and individual fitness issue would come into it perhaps if a population had a hard time finding easy prey and all of that potential for bite development stored up in the genome then allowed them to get MEAN and start chewing rocks to raise their fitness to survive testing times. It may well be that T.rex had such a varied diet that it's optimal bite force wasn't always maintained but was still genetically possible. I love Gould's essay on the Flamingo's smile, his discussion of behaviour and structural limitations is really far-reaching.. I'd recommend that one. In fact I'm off to read it my self.
Zach said…
I'd be interested to see what forces led to the evolution of more robust tyrannosaurs myself. There's certainly a distinct "gracile to hyper-robust" thing going on, from Alectrosaurus to Tyrannosaurus, with Albertosaurus, Appalachiosaurus, Daspletosaurus, and Tarbosaurus in between. I would suggest sexual selection and niche partitioning as possible factors.

Questions remain, however, How strong was Daspletosaurus' bite? What about Tarbosaurus? Tyrannosaurus'? Were they all living around different prey items? Were they ALL bone-crushers? In tyrannosaurs, does increased bite force = more prey choice?

You raise very good questions, brother, and it's what makes paleo so interesting!
I've got some really rough estimates of maximum bite forces for the larger tyrannosaurids:

Tyrannosaurus = 13900 - 16500 N
Tarbosaurus = 6100 N
Daspletosaurus = 5500 - 6500 N
Gorgosaurus = 3300 N

As far as previously published body mass estimates go, Daspletosaurus is a heavier animal than Tarbosaurus; and Tyrannosaurus is on average about twice as heavy as Daspletosaurus.

Lumped together with other theropod bite force estimates, and it's quite obvious that bite force scales as expected with body mass or in other words isometrically.

*My bite forces are estimated independent of body mass.
Zach said…
So then bite force wasn't necessarily "selected" among tyrannosaurs, but rather increased automatically as the animals became larger? That's interesting.

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