Gharials, dinosaurs, sexual selection, dimorphism, communication and conservation

Male (above) and female (below) gharial skulls. Photo courtesy of Larry Witmer.

So, yes, new paper time and which the concept behind this one was quite simple the outcome (as is so often the case) rather spiralled out into a bunch of other, very interesting aspects. As I noted in the run up to this post, I’ve been working a lot on sexual selection and what it means for dinosaurs in particular and wanted to use gharials as the perfect model for dinosaurs but lacked a dataset on these rare animals. A chance post by Larry Witmer led me to contact him about his dataset but it turned out to be only three animals, not the dozens I’d hoped for.

It was though, enough stimulus to get me hunting and with Jordan Mallon roped in with his interest in testing these ideas we just needed to get enough data. Happily, my former undergrad student Patrick Hennessey wanted to get engaged in some research and had time on his hands, so while I e-mailed every museum curator and croc research I could asking for photos of skulls, he set off to visit every collection in the south of the UK that was accessible. Some months later and we had an incredible set of over 100 specimens. We know of more too from photos that lacked scalebars (we were unuseable) or were in museums where we couldn’t get a response from the curator, or had various bits of skin preserved which concealed key bits of data. (We also found a good few mislabelled specimens of Tomistoma while we were at it). Still, 100 is a massive dataset for this kind of work and especially for such a rare animal and this gave us an excellent platform for our analyses.

Digging into the gharial literature though we soon found other issues. Despite the fame of these animals, their rarity means the literature on them is very small and very little is known in detail or was last written about in detail decades ago. To complicate things further, the two distinctive male traits (a fossa on the snout that correlates with the ghara, and a pair of palatal bullae) have never been truly convincingly shown to be definitively male accoutrements. Happily, an analysis of the data did suggest that the fossa was clearly a male feature and the bullae most likely were too.

Moving onto the central point of the project, analysis of the dataset showed that without pre-existing evidence for a given specimen being male or female, discovering any evidence of dimorphism was very hard, even for a dataset of over 100 animals. Gharials are strongly dimorphic in body size but the overlap between larger females and smaller males across much of the data, and the unknown sex of juveniles (which shown neither fossae nor bullae) makes finding this signal impossible. This matches what Jordan and I have said in a previous paper, and suggests that short of very large datasets and / or very strong dimorphsm (even more than seen here) or very good evidence for the sex of most specimens, it will be hard to find. That means that for the average data set we have for even well-represented species of dinosaurs (well under 100 incomplete specimens, no idea of levels of dimorphism but unlikely to be well above what we see in modern species, and no data on sex) we are not going to get a signal on dimorphism even if it’s there. I’m sure dimorphism is common in dinosaurs but I’m also sure we’re not finding it.

Female (left) and male (right) gharial snouts, the latter showing the expansion of the snout and the narial fossa anterior to the opening that makes the nares. Image courtesy of Larry Witmer.

That is, of course, based on things like body size or where a feature is expressed in both sexes (as, for example, ceratopsian fills appear to be). Presence-absence dimorphism (where one sex has a feature the other does not) should still show up relatively clearly with much smaller sets of data, but we’re not aware of any species that would obviously fit this criterion. The fossil record isn’t giving up numerous horn-less Allosaurus or dome-less Pachycephalosaurus specimens and while there are things like the two Khaan specimens with different tail anatomy, it’s just those two for now rather than a nice dataset of a dozen or so. Well-known taxa like Centrosaurus and Coelophysis are distinctly lacking in obvious dimorphism.

All of this is hopefully interesting and important for understanding sexual selection in the fossil record and as a guide for future research, but this work also threw up some interesting information for the gharials themselves which is worthy of comment. First of all, we were able to show that the fossa on the snout which is the correlate for the ghara is strongly positively allometric. This is no big surprise but it’s good confirmation that this feature is under sexual selection, and conforms with the (limited) evidence that the ghara starts growing around the time that these animals become sexually mature. We also note that it likely serves as an honest signal, since it would generate tremendous drag on the tip of the snout and that’s pretty critical for an animal with a super thin and presumably hydrodynamic set of jaws used to catch fish.

Surprisingly though, the bullae don’t show this pattern. They first appear on skulls around the same time as the fossa suggesting they are also linked to reproduction, but they first appear just before the fossa. We suggest that this is because the ghara while still small, may not need a fossa to hold it onto the skull and so the ghara and bullae may start growing at the same time, but the bullae would appear on the skeleton first. The bullae are also not allometric, so while they are larger in larger males, they are not disproportionately larger. This suggest that while they are an important part of the reproductive biology (and presumably as part of the palatal sinuses, potentially in making noise) it might be there merely to indicate sexual maturity rather than be an actual attractor. Either way, these give us some hints about the reproductive biology of these animals which gives us some hypotheses to test.

One last thing we spotted is that the very largest males are quite disproportionately robust. They have unusually wide skulls (including the normally slender snout) and also have very thick teeth, with animals only 20% smaller having teeth about half as thick. To our knowledge this has not been observed before and quite what this means isn’t certain. We hypothesise that these very large individuals might either have especially strong heads and teeth for fighting each other, or perhaps because they are entering a different niche and are able to exploit much larger prey than others. Either way, this points to an important issue given how endangered gharial populations are.

Very young gharials, yet to display any external features that might indicate their sex.

With animals under strong sexual selection, a few individual males will have a disproportionate amount of the mating opportunities in a population. But those males are also likely very well adapted to the prevailing conditions. They have, essentially, a good combination of genes allowing them to grow so big and maintain such a large ghara. If they are operating in a different niche and that isn’t taken into account (they may be eating much larger fish species compared to other gharial for example) when trying to protect them and conserve their habitats, then they might be especially vulnerable. If your genetically best adapted and fittest individuals are at most risk, that’s potentially very bad news and is unlikely to be good for the long term survival and genetic health of the population. This is of course, potentially rather speculative, but it’s supported by what we understand of strong sexual selection and the observations about the largest male skulls. It’s certainly something that is worth checking out in more detail and at the bare minimum it’s an interesting observation about their ontogeny and what that might mean for our taxonomy in the fossil record.

So here ends a very long process to analyse and assess dimorphism in gharials as a model for dinosaurs. It has thrown up far more complexity and nuance, especially in the living species themselves, than I ever thought but that has been in itself most interesting. It only remains for me to thank my coauthors for their contributions on this paper, and the huge number of curators and researchers who generously checked catalogues and sent in photos for us, the paper really would not exist with them all.

Hone, D.W.E., Mallon, J.C., Hennessey, P., & Witmer, L.M. 2020. Ontogeny of a sexually selected structure in an extant archosaur Gavialis gangeticus (Pseudosuchia: Crocodylia) with implications for sexual dimorphism in dinosaurs. Peer J.

 

Sexual selection in dinosaurs, the story so far…

I have a major new paper coming tomorrow on sexual selection in dinosaurs. This is an area in which I have been extremely heavily involved in the last decade and have published numerous papers on this subject with various colleagues, writing about the underlying theory of sexual selection and how it might appear in the fossil record, providing evidence for it and actively testing hypotheses. This has also led into my working on related issues of ontogeny and social behaviour in dinosaurs which feed back into these areas to try and deal with certain aspects that came up as a result of these analyses.

Suffice to say I’m not going to go back over the whole history of my work in the field, or that of plenty of other researchers which is both relevant and important. But a little bit of context is important with respect to the coming paper because it’s something that I’ve had in my mind to do for about as long as I’ve been working on this subject but I didn’t think I’d be able to do because the dataset didn’t exist.

All of the work I have done really tried to get into answer the questions of which features of which dinosaurs may have been operating under sexual selection and can we tell. (More properly, I should say socio-sexual selection since teasing out social dominance signals from sexually selected signals is probably impossible though mostly the two are more or less synonymous in various ways so it’s not a major issue conceptually). The short answer is that really quite a lot of features probably are under some form of sexual selection. We can see this by the fact that we can rule out functional explanations for things like ceratopsian crests as being anchors for muscles attachments, radiators, or for defence because they are highly variable and / or fundamentally don’t work (Elgin et al., 2008; Hone et al., 2012). They are costly traits to grow and lug around (be they stegosaur plates or hadrosaur crests) and so clearly have a fitness cost, ruling out species recognition as a signal (Knell et al., 2012; Hone & Naish, 2013). Similarly, there is no clear pattern of differentiation among sympatric species as would be critical for a recognition trait (Knapp et al. 2018). They are highly variable both within and between species, another hallmark of sexually selected traits (Hone & Naish, 2013; O’Brien et al., 2018) and finally they grow rapidly as animals reach sexual maturity which is absolutely characteristic of sexual selection (Hone et al., 2016; O’Brien et al., 2018).

The one issue that has remained elusive in all of this is the vexed issue of dimorphism. This has proven very hard to detect for a variety of reasons, but most notably the generally small sample sizes we have for dinosaurs and the tendency for males and females to overlap in size and morphology over much of their lifespan (Hone & Mallon, 2017). To top it off, mutual sexual selection can reduce or even eliminate dimorphism making it harder still to detect and meaning even an apparent absence of it, does not mean sexual selection is not in operation (Hone et al., 2012).

It would be nice to be able to explore the issue of dimorphism in particular in more detail with an extant analogue. Plenty of comparisons have been made to various living taxa in terms of dimorphism (be it body size or major features like a crest or sail) but they run into various issues. Mammals are nice and big and often have things like horns that differ between males and females (either in shape or presence / absence), but they’re phylogenetically very distinct and have the problem of growing quickly to adult size and staying there. Lizards offer something interesting with some dimorphic species with various signal structures (like some chameleons) but then while they are reptiles, most are small and the biggest varanids have no sexually selected structures. Birds are obviously literally dinosaurs but have a mammalian-like growth and are not very big. While there’s plenty of size dimorphism in them, there are few that have obviously dimorphic traits that would show up in the skeleton (like horns).

That leaves the crocodylians, which are off to a good start. Some are very large and take a long time to grown to adult size, all are egg layers, they are sexually mature long before full size meaning they would likely express sexually selected traits while still quite small (like dinosaurs and unlike birds or mammals), and a number are also sexually dimorphic in body size. The only thing missing is some kind of sexually selected bony feature, or at least one with a clear osteological correlate.

And so to the gharials, the wonderfully weird crocodylians of the Indian subcontinent which tick every single one of these boxes right down to the growth on the snout of males, the ghara, that is absent in the females. This has long been obviously the one taxon that ticks pretty much every possible box and would provide an excellent living model to analyse and see how easy (or not) dimorphism is to detect when you have a known dataset to work from. The obvious limit to this plan is that these animals are extremely rare and most museums have few, if any, specimens. The one species that was pretty much perfect for my plans immediately fell out of contention because I couldn’t see how I could get a dataset together that would be sufficient for analysis, so the idea was shelved. Until recently…

Obviously, to be continued.

 

Papers on sexual selection, dimoprhism, socio-sexual signaling, social behaviours and related subjects in fossil reptiles:

O’Brien, D.M., Allen, C.E., Van Kleeck, M.J., Hone, D.W.E., Knell, R.J., Knapp, A., Christiansen, S., & Emlen, D.J. 2018. On the evolution of extreme structures: static scaling and the function of sexually selected signals. Animal Behaviour.

Knapp, A., Knell, R.J., Farke, A.A., Loewen, M.A., & Hone, D.W.E. 2018. Patterns of divergence in the morphology of ceratopsian dinosaurs: sympatry is not a driver of ornament evolution. Proceedings of the Royal Society, Series B.

Hone, D.W.E., & Mallon, J.C. 2017. Protracted growth impedes the detection of sexual dimorphism in non-avian dinosaurs. Palaeontology, 60: 535-545.

Hone, D.W.E., Wood, D., & Knell, R.J. 2016. Positive allometry for exaggerated structures in the ceratopsian dinosaur Protoceratops andrewsi supports socio-sexual signaling. Palaeontologia Electronica, 19.1.5A.

Hone, D.W.E. & Faulkes, C.J. 2014. A proposed framework for establishing and evaluating hypotheses about the behaviour of extinct organisms. Journal of Zoology, 292: 260-267.

Hone, D.W.E., & Naish, D. 2013. The ‘species recognition hypothesis’ does not explain the presence and evolution of exaggerated structures in non-avialan dinosaurs. Journal of Zoology, 290: 172-180.

Knell, R., Naish, D., Tompkins, J.L. & Hone, D.W.E. 2013. Is sexual selection defined by dimorphism alone? A reply to Padian & Horner. Trends in Ecology & Evolution, 28: 250-251.

Knell, R., Naish, D., Tompkins, J.L. & Hone, D.W.E. 2013. Sexual selection in prehistoric animals: detection and implications. Trends in Ecology and Evolution, 28: 38-47.

Hone, D.W.E., Naish, D. & Cuthill, I.C. 2012. Does mutual sexual selection explain the evolution of head crests in pterosaurs and dinosaurs? Lethaia, 45: 139-156.

Taylor, M.T., 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.

Elgin, R.A., Grau, C., Palmer, C., Hone, D.W.E., Greenwell, D. & Benton, M.J. 2008. Aerodynamic characters of the cranial crest in Pteranodon. Zitteliana B, 28: 169-176.