Sexual selection – the phenomenon in which organisms compete over and choose mates on the basis of desirable traits – is one of the fundamental driving processes of evolution. It’s all around us, seemingly explains an enormous amount of the morphological and behavioural variation observed in the natural world, and has been shown to be tightly linked with speciation, adaptation, and even the susceptibility of a species to extinction. Accordingly, it is inherently logical to assume that sexual selection shaped the evolution of extinct animals as well as modern ones.

The latest contribution on this subject – that is, on the possible presence of sexually selected traits in fossil animals – has just been published by Robert Knell, myself, Joseph Tomkins and Dave Hone in Trends in Ecology and Evolution (or TREE). The article is only out as a digital preprint at the moment (Knell et al. 2012). Given that this article is about fossil animals in general (and not just about tetrapods) it includes some discussion (and illustration) of arthropods, fishy things and other animals (Knell et al. 2012). It’s a general review of this large and complex subject, pointing to the areas we might consider when thinking about sexual selection in fossil animals.

Those pesky archosaurs

The antlers of fossil deer, the horns of fossil bovids and rhinos, and the eyestalks of fossil stalk-eyed flies can – I think we can say with some confidence – be reliably interpreted as sociosexual organs just like those of living deer, bovid, rhino and stalk-eyed fly species. It’s those pesky archosaurs that are such a problem.

I’m of the opinion that many (or even most or even all) of the exaggerated structures present in dinosaurs and pterosaurs evolved under sexual selection pressure. I think this because I find the structures concerned (we’re talking cranial crests in hadrosaurs and pterosaurs, horns and frills in horned dinosaurs, and so on) analogous to sexually selected structures present in living animals. But the world is complicated, organs rarely have a single function, and other (sometimes competing) functions are not always absolutely ruled out.

On that note… feathers. The presence of elaborate plumes, tail-fans, streamers and racquet-like structures in some Cretaceous birds and bird-like maniraptoran theropods suggest that feathers were widely used in sexual display among these animals, as they are in birds today. As we note (Knell et al. 2012), data on the growth changes seen in oviraptorosaur forelimb feathers (Xu et al. 2010), and on the presence of feather iridescence in the deinonychosaur Microraptor (Li et al. 2012) add further support to the idea that these dinosaurs were using feathers in display. This doesn’t mean that everything about the early evolution of feathers was linked to display; nevertheless, the possible role of sexual selection in the early evolution of feathers is intriguing. It has been brought to my attention that we should have cited Richard Cowen and Jere Lipps’s book The History of Life in the context of this discussion, since they devoted a whole section of their book to the hypothesis that feathers may have originated as display structures and should be credited for explicitly proposing this hypothesis.

Incidentally, the article includes a reconstructed skull of the Asian lambeosaurine hadrosaur Olorotitan, redrawn from the original description. With classic timing, the monograph on Olorotitan has just appeared (Godefroit et al. 2012), and it makes the skull look somewhat different – it has a slender, more gracile snout and a deeper cranial crest. But that’s ok, the crest still has the elaborate form I was aiming to portray.

Our new article is one of several sexual selection projects I’ve been involved in. There’s the whole ‘the long necks of sauropods did not evolve primarily under sexual selection’ project (Taylor et al. 2011), and the mutual sexual selection one (Hone et al. 2012). Ontogenetic changes seen in the exaggerated structures of pterosaurs and other animals, coupled with the sheer extravagance and ‘non-functional’ nature of certain crests and other structures have also led me to argue that sociosexual display was the primary force directing the evolution of such structures (Naish & Martill 2003, Martill & Naish 2006).

Across all these pieces of research, there remains a fundamental and nagging question: how do we test for the presence of sexual selection in fossil animals? As we discuss (Knell et al. 2012), this is one of the main problems surrounding this issue. As indicated by my comment above, palaeontologists have mostly relied on analogy – that is, proposing a sexual selection function for a structure based on its general appearance and lack of ‘mechanical function’.

Information from ontogeny, data from the allometric changes that structures underwent during growth (Tomkins et al. 2010), and the inferred costliness of some of the relevant morphological traits seen in fossil animals all, we argue, appear more consistent with sexual selection than other explanations (Knell et al. 2012). But multifunctionality is never excluded. If the insane boomerang-shaped head of Diplocaulus was used in sexual display (as suggested by its growth trajectory: Rinehart & Lucas 2001), that doesn’t mean that it couldn’t also function in improving swimming performance (Cruickshank & Skews 1980).

The problem(s) with sexual dimorphism

Sexual dimorphism is an important indicator of sexual selection, but – as Dave, Innes Cuthill and I showed in our work on mutual sexual selection (Hone et al. 2012) – it’s not required, and it’s absent in some living animals that use exaggerated structures in sexual selection. Furthermore, there are some organisms (like spiders and echiuran worms) where pronounced sexual dimorphism is not clearly linked to sexual selection.

Palaeontologists always have sexual dimorphism in mind when looking at specimens thought to belong to the same taxon. Occasionally, we get really, really lucky and discover ridiculous things like numerous specimens of a species where some individuals have crests, some don't, and where at least one crestless specimen is preserved with an egg right next to its pelvic girdle (Lü et al. 2011).... more normally, however, such evidence is lacking and sample size is a massive problem. We know from living animals that individuals of both sexes overlap in measurements and proportions, and can only be reliably distinguished in robust statistical terms when large sample sizes are available. Oh, and the specimens don’t just have to be numerous, but also nicely preserved, and often three-dimensional as well. Good luck, then.

At the background of this research is the claim from some palaeontologists that the elaborate ornaments of dinosaurs and pterosaurs (and perhaps other fossil animals as well) functioned as ‘species identification’ badges, and that sexual selection fails as an explanation. Padian & Horner (2011a) argued that sexual selection couldn’t be at play in Mesozoic dinosaur lineages because sexual dimorphism appears to be absent: needless to say, this line of argumentation is dependent on the rejection of the existence of mutual sexual selection. Padian and Horner’s rejection of mutual sexual selection is based on the fact that Darwin regarded sexual dimorphism as a necessary prerequisite of sexual selection (Padian & Horner 2011a, b). I’m not alone in finding this an unsatisfactory position (Knell & Sampson 2011, Mendelson & Shaw 2012).

Furthermore, the ‘species identification’ hypothesis fails to credit the fact that ‘species recognition’ has yet to be supported as the key mechanism explaining trait evolution in modern animals that possess elaborate structures – instead, the structures concerned mostly have roles in sexual selection.

Excelsior!

Anyway, hopefully, Knell et al. (2012) will be seen as a useful review of sexual selection as it applies to palaeontology, and let’s hope that it inspires future research and the exploration of various of the problem areas we point to. There’s more to come.

Knell et al. (2012) has been discussed elsewhere in the blogosphere already. Dave Hone covered it here at his Archosaur Musings and Brian Switek just wrote about it here at Dinosaur Tracking. To see the original, uncropped version of the ridiculous brachiosaur reconstruction shown above, go here. For previous articles on some of the issues mentioned here, see…

Refs - -

Cruickshank, A. R. I. and Skews, B. W. 1980. The functional significance of nectridean tabular horns (Amphibia: Lepospondyli). Proceedings of the Royal Society of London, series B: Biological Sciences 209, 513-537.

Godefroit, P., Bolotsky, Y. L. & Bolotsky, I. Y. 2012. Osteology and relationships of Olorotitan arharensis, a hollow-crested hadrosaurid dinosaur from the latest Cretaceous of Far Eastern Russia. Acta Palaeontologica Polonica 57, 527-560.

Hone, D. W. E., Naish, D. & Cuthill, I. C. 2011. Does mutual sexual selection explain the evolution of head crests in pterosaurs and dinosaurs? Lethaia 45, 139-156.

Knell, R. J., Naish, D., Tomkins, J. L. & Hone, D. W. E. 2012. Sexual selection in prehistoric animals: detection and implications. Trends in Ecology and Evolution DOI: 10.1016/j.tree.2012.07.015.

- . & Sampson, S. 2011. Bizarre structures in dinosaurs: species recognition or sexual selection? A response to Padian and Horner. Journal of Zoology 283, 18-22.

Li, Q., Gao, K.-Q., Meng, Q., Clarke, J. A., Shawkey, M. D., D’Alba, L., Pei, R., Ellison, M., Norell, M. A. & Vinther, J. 2012. Reconstruction of Microraptor and the evolution of iridescent plumage. Science 335, 1215-1219.

Lü, J., Unwin, D. M., Deeming, D. C., Jin X, Liu, Y., & Ji, Q. 2011. An egg-adult association, gender, and reproduction in pterosaurs. Science 331, 321-324.

Martill, D. M. & Naish, D. 2006. Cranial crest development in the azhdarchoid pterosaur Tupuxuara, with a review of the genus and tapejarid monophyly. Palaeontology 49, 925-941.

Mendelson, T. C. Shaw, K. L. 2012. The (mis)concept of species recognition. Trends in Ecology and Evolution 27, 421-427.

Naish, D. & Martill, D. M. 2003. Pterosaurs – a successful invasion of prehistoric skies. Biologist 50 (5), 213-216.

Rinehart, L. F. & Lucas, S. G. 2001. A statistical analysis of a growth series of the Permian nectridean Diplocaulus magnicornis showing two-stage ontogeny. Journal of Vertebrate Paleontology 21, 803-806.

Padian, K. & Horner, J. R. 2011a. The evolution of ‘bizarre structures’ in dinosaurs: biomechanics, sexual selection, social selection or species recognition? Journal of Zoology 283, 3-17.

- . & Horner, J. R. 2011b. The definition of sexual selection and its implications for dinosaurian biology. Journal of Zoology 283, 23-27.

Taylor, M. P., Hone, D. W. E., Wedel, M. J. & Naish, D. 2011. The long necks of sauropods did not evolve primarily through sexual selection. Journal of Zoology 285, 150-161.

Tomkins, J., LeBas, N., Witton, M., Martill, D., & Humphries, S. 2010. Positive allometry and the prehistory of sexual selection. The American Naturalist 176, 141-148.

Xu, X., Zheng, Z. & You, H. 2010. Exceptional dinosaur fossils show ontogenetic development of early feathers. Nature 464, 1338-1341.