Why were elaborate cranial ornaments so diverse and so widespread in pterosaurs and Mesozoic dinosaurs? These structures – grouped together here as ‘cranial crests’ – vary markedly in form and position: they range from the semi-circular blades and keels present at the snout-tips of ornithocheiroid pterosaurs to the hollow tubes, fans and plate-like crests of lambeosaurine hadrosaurs and the bony frills of ceratopsians. Horns, hornlets, bosses, twin ridges and other structures decorate the skulls of various ornithischians and Mesozoic theropods, various pterosaurs possess sail-like crests, there are the thick skull domes of pachycephalosaurs, and so on. We can say with confidence that cranial ornamentation was common, if not ubiquitous, across Ornithodira (the clade of archosaurian reptiles that includes dinosaurs and pterosaurs).

A couple of weeks ago, Dave Hone, Innes Cuthill and I published our new paper on ornithodiran cranial crest function (Hone et al. 2011*). While there’s a fairly extensive literature on the anatomy and possible function of specific ornithodiran cranial crests, reviews of ornithodiran cranial ornamentation as a whole are surprisingly rare. As we’ll see here, our article isn’t just a review – our main aim is to bring a previously overlooked evolutionary phenomenon to broader attention.

* Because the dead tree version of the paper will appear this year, the paper will mostly be cited in future as ‘Hone et al. 2012’. That version hasn’t appeared yet, so for now I’m citing the digital version. We live in a stupid world where technical papers now have two different publication dates. In my opinion, ‘digital publication’ should be synonymous with ‘publication’.

Cranial crests and what to do with them

Which selective processes might have led to the evolution of all these crests? Here I need to add the caveat that we mostly ignored crests that seem to have become enlarged due to their role in anchoring muscles, like the sagittal and nuchal crests that are often big and obvious in muscle-headed primates, carnivorans, turtles, chameleons and so on (the caveat to this caveat is that such crests can provide information on fitness, and may then become exaggerated due to a role in sexual selection) [adjacent photo by Mila Zinkova].

As for the remaining cranial crests we see in fossil ornithodirans, their diversity is such that they can’t possibly all have had the same evolutionary history. Indeed, over the years, people have suggested that thermoregulation, acoustics or defence against predators encouraged the evolution of crests in specific lineages; more outlandish ideas include that lambeosaurine crests functioned as snorkels or air tanks or as specialised foliage deflectors, and that pterosaur crests functioned as sails or rudders.

Furthermore, the behavioural diversity and plasticity we see in living animals makes it likely or inevitable that ornithodiran crests were multi-functional: that is, used in diverse ways by the animals when they were alive. Consider that deer antlers aren’t just used in intraspecific fighting and display, but also in fending off predators, as tools for applying mud and parting vegetation, in thermoregulation and (perhaps, in Moose Alces alces) acoustics. Cassowary casques seem to be used in intraspecific display, but the birds also use them as foliage deflectors, as tools for moving forest-floor debris (Folch 1992), and perhaps even as ‘microphones’ for the collection of infrasonic calls (Mack & Jones 2003). With this multi-functionality permanently in mind, the challenge is to work out which proposed function represents the ‘primary driving force’ behind the evolution of the structure, and which functions were secondary or incidental. This is sometimes a surprisingly difficult issue to resolve, even in living animals.

In recent decades people have made efforts to test various of the functional hypotheses suggested for ornithodiran cranial crests. Several of the proposed ‘functional’ hypotheses can be rejected right off the bat as they were obviously ridiculous to start with (example: that Parasaurolophus used its tubular crest as a snorkel), and others don’t withstand scrutiny (examples: that tapejarid pterosaur crests functioned as windsails, that thalassodromid pterosaur dentary crests were specialisations for skim-feeding, or that thalassodromid premaxillary crests were special thermoregulatory organs) (e.g., Humphries et al. 2007, Elgin et al. 2008, Hone et al. 2011). Other proposals – I’m thinking here of the head-butting or flank-butting proposed for pachycephalosaurs – remain the subject of substantial argument.

So, these ‘functional’ hypotheses mostly haven’t worked out. And the fact that ornithodiran crests are often outlandish and appear well suited for visual display, combined with the fact that dinosaurs and pterosaurs seem in any case to have been visually oriented animals with excellent colour vision, has mostly led researchers to argue that ornithodiran cranial crests evolved primarily under selection for visual display.

The problem with sex (or with sexual dimorphism, anyway)

Could these crests have been used in sexual display? That is, that males showed off to attract females? Yes, vice versa could apply but - since female showiness is rarer in the modern world than male showiness - it seems reasonable to assume that this was the case in the Mesozoic world as well. What seems to be sexual dimorphism is present in the pterosaurs Pteranodon (where big individuals have narrow pelvic girdles and long, pointed crests and smaller individuals have wide pelvic girdles and short, blunt crests) and Darwinopterus (where same-sized individuals come in crested and crestless forms, and a crestless individual is preserved in indisputable association with an egg).

However, sexual dimorphism is difficult or impossible to detect in members of some other ornithodiran lineages. It has been argued that sexual dimorphism is present in the domes of some pachycephalosaurs and in the frill and horn shapes of such ceratopsians as Protoceratops and Agujaceratops. However, this supposed dimorphism is either extremely subtle and difficult to be confident about (in Agujaceratops it concerns minor differences in the divergence angles of the brow horns and the orientation of the frill with respect to the rest of the skull ), or just about continuous across the supposed ‘sexes’ and quite plausibly merely a representation of intrapopulational variation (in Protoceratops, supposed males and females grade into one another via a series of intermediates). With the caveat in mind that sample size is nearly always a problem with fossil species, we can say with relative confidence that we have a number of dinosaur and pterosaur taxa where largish numbers of specimens fail to reveal convincing dimorphism.

The conclusion must be that - for a reasonable number of crested dinosaurs and pterosaurs - males and females were similarly ornamented, with similarly sized, similarly elaborate cranial crests present in both adult males and adult females. If cranial crests evolved primarily under selection for visual display, and if males and females are equally ornamented, could it be that the ornaments are species recognition devices? That is, that the crests were used as badges to distinguish, say, adult individuals (of both sexes) of Corythosaurus casuarius from adult individuals (of both sexes) of the contemporary lambeosaurine Lambeosaurus lambei. While this is the most commonly encountered hypothesis used to explain the presence of similar male and female display traits, it’s problematic (more on this below). And there’s another possible explanation for mutual ornamentation; surprisingly, it’s been near totally ignored in the palaeontological literature until now.

Mutual sexual selection comes to palaeontology (at last)

Do we see visual display structures that are similarly expressed, and similarly elaborate, in both males and females anywhere in the modern world? Yes we do, in a wide diversity of modern bird and lizard species, and also in certain fish, insects and other taxa (we'll look at the specific taxa involved in a moment). Herein we find the phenomenon of mutual sexual selection, first proposed as a mechanism of mate choice by Julian Huxley in 1914 (and alluded to by Darwin in his 1871 The Descent of Man, and Selection in Relation to Sex).

There’s an extensive technical literature on mutual sexual selection (MSS from hereon); it’s uncontroversial, well accepted and well researched (for reviews, see Amundsen 2000, Bonduriansky 2001, Hooper & Miller 2008), and it fits conformably into our wider understanding of sexual selection theory.

MSS is best known in birds and was initially proposed to explain the evolution of mutual ornaments in the Great crested grebe Podiceps cristatus (Huxley 1914). Other bird species in which MSS seem to be present include Black swans Cygnus atratus, where both males and females possess peculiar curled wing feathers (Kraaijeveld et al. 2004a), European starlings Sturnus vulgaris, where males and females both select mates on the basis of their iridescent throat feathers (Komdeur et al. 2005), and Crested auklets Aethia cristatellus, where males and females both evaluate potential mates on the size and quality of their forehead crests (Jones & Hunter 1993). Some authors even suggest that MSS may operate in just about all of those birds where males and females are brightly coloured and/or highly ornamented. The list might therefore include tropicbirds, some parrots (Platycercus and Trichoglossus), some herons, puffins, bee-eaters, certain sunbirds, paradise kingfishers (Tanysiptera), some Neotropical jays (Cyanocorax and Calocitta) and certain tyrant flycatchers (Muscivora) (Jones 1992).

MSS has also been reported in fruit flies (Chenoweth & Blows 2003), mosquitoes (South & Arnqvist 2011), sticklebacks (Bergstrom & Real 2000), pipefishes (Widemo 2003), agamid lizards (Ord & Stuart-Fox 2005) and others. Some workers have suggested that it may prove “to be much more common than we think” (Bergstrom & Real 2000, p. 494).

All of this makes it rather surprising that the possible presence of MSS in Mesozoic ornithodirans has, until now, gone unmentioned and unconsidered (with two exceptions that we know of: Tomkins et al. (2010) and Taylor et al. (2011)). And here we find the main thrust of our new paper. Dave, Innes and I briefly evaluate existing hypotheses of cranial crest presence in Mesozoic ornithodirans, discuss the occurrence of mutual ornamentation in the males and females of certain Mesozoic ornithodiran species, and ask the question: were Mesozoic dinosaurs and pterosaurs practising mutual sexual selection? (Hone et al. 2011).

Those with good memories might note that we actually presented this idea to the Mesozoic ornithodiran research community back in 2007 (for proof, see the Tet Zoo ver 2 article The Wellnhofer pterosaur meeting, part I). Furthermore, a brief discussion of MSS is included in the ‘necks for sex’ rebuttal that Dave and I published recently with Mike Taylor and Matt Wedel (Taylor et al. 2011).

Why does MSS evolve?

As we note in the paper (Hone et al. 2011), the concept of MSS fits into a larger picture in which mate choice is more complex than often assumed, and in which the interplay between sexual selection, ecology and natural selection has to be considered. Sexual selection is not just about gaudy males that act as ‘copulation maximisers’: intrasexual competition occurs in females as well as males, and sexual dimorphism is not a defining hallmark of sexual selection. Indeed, why might MSS have evolved in the first place?

Perhaps the most familiar explanation is that male ornaments become expressed in females for nonadaptive, incidental reasons explained by developmental or genetic correlation between the sexes. This seems like a nice idea, but it’s unlikely to be widely applicable as species seem to mostly avoid this problem by evolving obvious sexual differences. Note, however, that genetic correlation has been demonstrated in Barn owls Tyto alba (where plumage spottiness in males is correlated with such factors as reproductive success and the size of the heart: Roulin et al. 2001) [adjacent photo by Peter Trimming].

Might mutual ornamentation have evolved because it proves advantageous in winning disputes over territory or resources? Data from mutually ornamented swans, sparrows and antbirds indicates that MSS partially results from competition over resources, with permanent showy ornaments playing a role in female-female disputes (West-Eberhard 1979, 1983, Kraaijeveld et al. 2004b, Tobias et al. 2011). This is known as the social selection hypothesis, and it’s supposedly more to do with resource defence and conflict with conspecifics than sexual selection. However, it’s complicated by the fact that mate choosiness, and hence sexual selection, contributes to the presence of mutual ornamentation in the species concerned.

So - how about the possibility that female ornamentation has primarily evolved under sexual selection pressure, like that of males? In some species exhibiting MSS, like certain pipefishes, males play a substantial role in parental care and hence need to be choosy about the qualities of the individual providing the eggs. Females thus need to be showy just as males do. Monogamous species where both parents contribute to parental care also need to be choosy about their partners. The evolution of MSS is associated, therefore, with species where both sexes are working hard to advertise their quality via sexual signalling. As discussed above, MSS seems to explain the mutual ornamentation present in a diverse number of insect, fish, lizard and bird species.

When it comes to Mesozoic ornithodirans, we don’t really know much/anything about the contributions made to reproduction and parenting by the different sexes (though substantial male investment has been suggested for non-avialan maniraptorans… not without controversy, though). However, the fact that birds are phylogenetically close to Cretaceous dinosaurs, the fact that bird-like visual ornaments seem to have evolved in some Cretaceous theropods, and the fact that various pieces of evidence indicate complex, frequent social behaviour in Mesozoic ornithodirans all make it likely that sexual selection, and specific kinds of sexual selection like MSS, was a common factor in ornithodiran evolution.

In quest of alternative explanations

In recent years, the role that visual signals might have played in the evolution of Mesozoic dinosaurs has become an increasingly popular topic and some fairly heated exchanges on the topic have occurred in the literature (Knell & Sampson 2011, Padian & Horner 2011a, b, Taylor et al. 2011).

One explanation for the presence of species-wide cranial ornamentation is that the structures concerned evolved as species recognition devices. This idea seems logical when we think of, say, the contemporaneous hadrosaur and ceratopsian species that lived in close proximity in Campanian Laramidia. However, there are several flaws in the species recognition hypothesis. One is that modern sympatric species seem able to recognise conspecifics on the basis of often subtle features of pigmentation, shape and size, and via differences in acoustic and/or olfactory signals (in other words, the growth and maintenance of a giant, costly crest is not required). Another is that the crested ornithodirans we know about don’t consistently live alongside relatives that could serve as potential sources of confusion. And what about those species that did live alongside highly similar close relatives and yet didn’t possess these species recognition ‘badges’? Furthermore, cranial ornaments in living species don’t – so far as we know at the moment – work as ‘species identifiers’ (Knell & Sampson 2011).

What about the idea that cranial ornaments could act as social signals, or status signals, within crested species? That is, that they signalled sexual maturity and the move away from juvenile status? This idea is often mentioned in papers on pachycephalosaurs and ceratopsians, and some authors even say that ‘social signalling’ of this sort better explains ornithodiran ornamentation than does sexual selection. However, the use of a signal as a maturity indicator is very obviously compatible with the use of the same signal as a sexual signal, especially in view of MSS. In fact, the existence of apparently distinct juvenile phases in cranial ornamentation (as reported for, say, Triceratops) is a fairly obvious requirement for the existence of sexual selection: individuals have to make the transition from non-sexual to sexual at some point during ontogeny.

More and more and more to think about

There are actually many areas of our paper that could warrant elaboration here. One concerns feathers. Cranial ornaments aren’t entirely absent in feathered theropods (oviraptorids, cassowaries, guans, curassows, helmeted guineafowl and so on), but they do seem rarer relative to their prevalence in non-feathered theropods. Could – we suggest (Hone et al. 2011) – feathers have mostly ‘replaced’ bony cranial ornaments during theropod evolution? After all, feathers are cheaper for lots of reasons.

Then there’s the whole sauropod neck thing. Sauropodomorph cranial ornamentation appears rare (though note that possible ornamentation is present in at least some taxa, as illustrated here), so might neck length have been controlled by sexual selection, as one author has proposed? Dave and I worked with Mike Taylor and Matt Wedel to examine this question in a previous study (Taylor et al. 2011), so I don’t think I need to talk about it any more.

And what about ornament loss? As we note (Hone et al. 2011), brow horns were strongly reduced and even lost in some ceratopsian lineages. If ceratopsian horns evolved within the context of sexual selection, how do we explain their reduction and loss in some lineages? Sexually selected traits like horns, elaborate tail feathers and brightly coloured display patches have repeatedly been lost in certain lizard, bird and fish groups where sexually selected display structures are otherwise ubiquitous (Wiens 2001).

Quite why these repeated losses occur remains controversial: it might be an adaptive response to life in a new environment (visual display structures, for example, are of little use if you start living in a habitat where visual cues can rarely be used), or it can be caused by a new limitation in resources (reduced carotenoid availability, for example, causes some passerine birds to lower or lose the intensity of their pigmentation).

Studies on guppies and swordtails indicate that sympatry with similarly ornamented species can cause females of one species to prefer reduced or absent ornamentation in the males of their own species, and pressure among males finches and phrynosomatid lizards to avoid aggressive interactions and tone down their level of territoriality also seems to have resulted in a reduction or loss of male ornaments. The point I’m making here is that ornament reduction and/or loss is completely compatible with the role of these structures in sexual selection. [In the adjacent image, the Palawan peacock-pheasant photo is by Dante Alighieri; the Bronze-tailed peacock-pheasant image is from Hume & Marshall’s 1880 Gamebirds of India, Burmah, Ceylon.]

Well done, you’ve made it to the end of this article

As you might have realised given the length of this article, there are lots of confusing, complicated and overlapping facets to the possible existence of MSS in Mesozoic ornithodirans, and of the phenomenon of mutual ornamentation, sexual selection and social and status signalling as a whole.

Does our proposal provide an answer to the prevalence and repeated evolution of cranial crests in Mesozoic ornithodirans? No, of course not: our article is a discussion piece, serving predominantly to bring the phenomenon of MSS to the attention of a wider range of palaeozoologists. And how might we begin to test for the presence of MSS in these fossil species, seeing as all we do in our paper is say that Mesozoic ornithodirans look well equipped for MSS to be in action? These are really exciting times for anyone interested in sexual selection, ontogeny and reproductive biology in Mesozoic archosaurs. This new contribution is hardly going to be the last word on the subject, and a great deal of work remains to be done.

Dave Hone has also blogged about our new paper here (he was, err, somewhat more terse in his article than I have been here). Ask if you want the pdf (or, if you have the means, download here).

For previous Tet Zoo articles on the reproductive and social behaviour of Mesozoic dinosaurs and pterosaurs, please see...

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