Ceratopsian horns and frills – what drove their evolution?

So I have another new paper out on sexual selection and what this means for dinosaurs. This one has been led by my PhD student Andy Knapp (follow him on Twitter here) and he agreed to write about it here:

Ceratopsians are among the most instantly recognisable dinosaurs thanks to their enormous, elaborately-adorned skulls. The frills and horns of ceratopsians have been the subject or ongoing debate in palaeontological circles since the discovery of Triceratops in the late 19th century. Triceratops is known to everyone, specialists and non-specialists alike, and remains the classic example of ceratopsian skull morphology, with three large forward-pointing horns and a thick, shield-like frill extending back from the rear of the skull. It seemed obvious to early palaeontologists that these features had evolved for protection. The trouble is that Triceratops is almost alone in possessing this precise combination of features. Many of the larger ceratopsians that we know of didn’t have such large horns, and most had large, weight-saving fenestrae in their frills which would offer little protective value in life. In recent years the large number of known ceratopsian species has increased with a steady stream of new discoveries, each with its own characteristic horn and frill morphologies. These discoveries have posed a whole load of new questions as to what their purpose was.

Large, elaborate features with no obvious use – such as the frills and horns seen in ceratopsians – are expensive to grow and maintain, and obvious parallels in living creatures involve sexually selected features. The most extravagant examples of sexually selected features, as realised by Darwin in his book The Descent of Man, involve extreme sexually dimorphism in traits and/or overall size; peacock tails, elephant seals, etc. In contrast, there is no convincing evidence of sexual dimorphism in any ceratopsian taxa. This has led some researchers to reject the hypothesis of sexual selection as an explanation for exaggerated features in ceratopsians and other dinosaurs, and suggest that instead these features have evolved for species recognition.

Species recognition is the idea that being able to differentiate members of your own species is vital in herding, protection and mating. Basic examples of ‘species recognition’ are everywhere in nature; zebras don’t have trouble telling lions apart from other zebras! The more specific idea that physical traits evolve as a mechanism to allow differentiation is controversial. There are a few known examples of divergence of traits in closely-related taxa where hybridisation could be detrimental to fitness, a process known as reproductive character displacement. This is distinct from ecological character displacement, where sympatric taxa that fill similar ecological niches diverge in traits associated with resource acquisition. The rock nuthatches Sitta neumayer and S. tephronota exist across central Asia in partially overlapping ranges. Where they are sympatric, the distinctive dark eye stripe, ubiquitous across the rest of the two species’ ranges, fades in intensity in the population of S. neumayer. This has been interpreted as an adaptation to prevent hybridisation between the two species. Crucially, other known examples of reproductive character displacement involve minor modifications to pre-existing, often sexually selected features.

Reproductive character displacement is not expected to operate where a taxon exists in isolation, because there is no evolutionary pressure for traits to diverge. This prediction allows us to test the hypothesis of species recognition as an explanation for the presence of distinctive traits in extinct taxa for which we have good geographical information. Ceratopsians fit these criteria well. They were widespread across North America and Asia, speciose, and many species are known from relatively complete remains. We compiled and assessed a list of 350 cladistic character traits for a 46 well-known ceratopsian species and compared how the traits generally considered ornamental, and thus contenders to be species recognition traits, varied between sympatric and non-sympatric species. We also examined at other traits; those that were internal and therefore not visible during the animal’s life, and those that were external but not considered to function as a display trait. We then conducted a pairwise comparison of each possible species pair for three distinct character classes; internal, display, and external non-display.

We then compared the results for species pairs known to be sympatric and, therefore, likely to encounter one another in life, with non-sympatric species pairs. For each category we found increasing character divergence with increasing phylogenetic distance as expected, but, crucially, found no difference between the disparity of the display characters of sympatric species and those of non-sympatric species. This suggests that interaction between species has no effect on the evolution of ornaments in ceratopsians, and that species recognition is not a contributing factor to ornament evolution. Of course, it is entirely plausible that ceratopsians were able to identify conspecifics by their ornamentation, but this would have been a byproduct of ornamentation, not a cause.

The ruling out of species recognition as a driver of ornament evolution, at least in ceratopsians, shortens the list of possible explanations. Avoiding hybridisation would benefit both parties and so the evolution of distinguishing features should tend towards a zero-cost exercise. In contrast, ceratopsian skulls are the largest of any terrestrial vertebrate and impose certain limitations on their bearers. Computer models of ceratopsians have shown their massive skulls shifted their centre of mass further forwards than other quadrupedal dinosaurs. Compared with the hadrosaurs that they shared the ancient river deltas of what is now Canada’s Dinosaur Provincial Park, this made them poor swimmers and liable to drown when crossing bodies of water. This obvious handicap, along with the sheer cost of growing and maintaining such a large component of overall body mass that has no obvious mechanical or ecological function, points to an explanation that favours investment in high-cost structures.

An additional result of our analysis was that at the lowest phylogenetic distances, ornamental traits were around ten times more diverse than internal traits and three times more diverse than non-ornamental external characters. This suggests a general trend for rapid evolution of ornamental traits. Rapid evolution and high-cost are both hallmarks of sexually selected features. If the frills and horns of ceratopsians are sexually selected, as has been previously suggested, they are distinct from extant taxa in being both highly exaggerated and sexually monomorphic. This combination suggests strong sexual selection that applies more-or-less equally to both sexes. Some evidence for ceratopsian ornamentation being sexually selected has been demonstrated previously, and this study both adds to this evidence and rejects a competing hypothesis. Ultimately, our findings open up further avenues for exploring the life history and ecology of these fascinating and enigmatic creatures.

Knapp A, Knell RJ, Farke AA, Loewen MA and Hone DWE (2018). Patterns of divergence in the morphology of ceratopsian dinosaurs: sympatry is not a driver of ornament evolution. Proc. R. Soc. B. 20180312. http://dx.doi.org/10.1098/rspb.2018.0312

References

Brown WL and Wilson EO (1956) Character displacement. Systematic Zoology. 5: 49-64

Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. London, John Murray

Henderson DM (2014). Duck Soup: The floating fates of hadrosaurs and ceratopsians at Dinosaur Provincial Park, in Eberth D and Evans D (eds). Hadrosaurs. Bloomington: Indiana University Press. pp. 459-466

Hone, D.W.E., Wood, D., and Knell, R.J. (2016). Positive allometry for exaggerated structures in the ceratopsian dinosaur Protoceratops andrewsi supports socio-sexual signalling. Palaeontologica Electronica. 19.1.5A: 1-13

Knell RJ, Naish D, Tompkins JL, and Hone DWE (2012). Sexual selection in prehistoric animals: detection and implications. Trends in Ecology and Evolution. 28; 38 – 47

Maidment SCR, Henderson DM, and Barret PM (2014). What drove reversions to quadrupedality in ornithischian dinosaurs? Testing hypotheses using centre of mass modelling. Naturwissenschaften. 101: 989 – 1001

Padian, K. and Horner, J.R. (2010). The evolution of ‘bizarre structures’ in dinosaurs: biomechanics, sexual selection, social selection or species recognition? Journal of Zoology. 283; 3 – 17