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Did dinosaurs and pterosaurs practise mutual sexual selection?

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A selection of crested non-avialan theropod and ornithischian dinosaurs. Diagrams by Dave Hone.

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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’.

A selected of crested pterodactyloid pterosaurs. A. Ornithocheirid ornithocheiroid Ornithocheirus. B. Tapejarid azhdarchoid Tapejara. C. Thalassodromid azhdarchoid Tupuxuara. D. Dsungaripterid Dsungaripterus. E. Pteranodontid ornithocheiroid Pteranodon. F. Nyctosaurid ornithocheiroid Nyctosaurus. Diagrams by Dave Hone.

Cranial crests and what to do with them

Male Western gorilla (Gorilla gorilla): that's quite the sagittal crest. Photo by Mila Zinkova, from wikipedia.

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.

Cassowaries: sometimes very hard to see in dimly lit forests. I wonder if the naked skin shows up better if you can see the UV part of the spectrum?

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.

Cassowaries! A selection of forms (now mostly regarded as part of Bennett's cassowary C. bennetti) from Walter Rothschild's seminal 1900 monograph.

Thalassodromeus depicted as a skim-feeder: a terrible, terrible idea. llustration by Maurilio Oliveira.

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)

Sexual dimorphism in the pterosaur Darwinopterus modularis, fantastically illustrated by Mark Witton.

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).

Purported sexual dimorphism in Protoceratops andrewsi, with the 'male' above, and 'female' below. From Dodson (1976).

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)

Great crested grebe courtship displays, as illustrated by Huxley (1914).

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 in action in (A) Crested auklet and (B) Black swan. (C) Curled wing feathers present in both male and female Black swan. From Hone et al. (2011).

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?

SHREEE!!! Tyto alba. Photo by Peter Trimming, from wikipedia.

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.

Big momma... or big dadda? Some authors have argued that dinosaurs found associated with nests and eggs, like this oviraptorid, were most likely males.

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).

Hadrosaur phylogeny, as reconstructed for Halstead's 1975 The Evolution and Ecology of the Dinosaurs. At this time, numerous forms now regarded as juveniles or variants were classified as distinct species. The phylogenetic relationships shown here haven't stood up to scrutiny. Click to enlarge.

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.

Ontogenetic sequence proposed for Triceratops by Horner & Goodwin (2006) (though produced prior to the proposal that Torosaurus may represent the 'ultimate' morph in the sequence). The juveniles look distinctive here, but the sequence we have is entirely consistent with sexual selection as the primary mechanism driving the evolution of the ornamentation.

More and more and more to think about

Bony crest (marked with asterisk) and feather distribution in theropods, from Hone et al. (2011). Click to enlarge.

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.

Skull of the titanosauriform sauropod Giraffatitan brancai, by Dave Hone. Look: a cranial crest (of sorts).

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).

Phylogenies show that the less ornamented Bronze-tailed peacock-pheasant (Polyplectron chalcurum), shown at bottom, lost much of its ornamentation and evolved from a far more elaborate species, like the Palawan peacock-pheasant (P. napoleonis), shown above.

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

Two of the authors critically examine a life-sized model of a thalassodromid pterosaur. All part of their extensive research.

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…

Refs – -

Amundsen, T. 2000. Why are female birds ornamented? Trends in Ecology & Evolution 15, 149-155.

Bergstrom, C. T. & Real, L. A. 2000. Towards a theory of mutual mate choice: lessons from two-sided matching. Evolutionary Ecology Research 2, 493-508.

Bonduriansky, R. 2001. The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biological Reviews 76, 305-339.

Chenoweth, S. F. & Blows, M. W. 2003. Signal trait sexual dimorphism and mutual sexual selection in Drosophila serrata. Evolution 57, 2326-2334.

Dodson, P. 1976. Quantitative aspects of relative growth and sexual dimorphism in Protoceratops. Journal of Paleontology 50, 929-940.

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.

Folch, A. 1992: Family Casuariidae (Cassowaries). In Del Hoyo, J., Elliott, A. & Sargatal, J. (eds). Handbook of the Birds of the World. Volume 1: Ostriches to Ducks. Lynx Edicions, Barcelona, pp. 90-97.

HONE, D., NAISH, D., & CUTHILL, I. (2011). Does mutual sexual selection explain the evolution of head crests in pterosaurs and dinosaurs? Lethaia DOI: 10.1111/j.1502-3931.2011.00300.x

Hooper, P. L. & Miller, G. F. 2008. Mutual mate choice can drive costly signalling even under perfect monogamy. Adaptive Behavior 16, 53-69.

Horner, J. & Goodwin, M. B. 2006. Major cranial changes during Triceratops ontogeny. Proceedings of the Royal Society, London B 273, 2757-2761.

Humphries, S., Bonser, R. H. C., Witton, M. P. & Martill, D. M. 2007. Did pterosaurs feed by skimming? Physical modelling and anatomical evaluation of an unusual feeding method. PLoS Biology 5, 1-9.

Huxley, J. 1914. The courtship habits of the Great Crested Grebe (Podiceps cristatus); with an addition to the theory of sexual selection. Proceedings of the Zoological Society of London 35, 491-562.

Jones, I. L. 1992. Sexual selection and the evolution of extravagant traits in birds: problems with testing good-genes models of sexual selection. The Auk 109, 197-199.

- . & Hunter, F. M. 1993. Mutual sexual selection in a monogamous seabird. Nature 362, 238-239.

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

Komdeur, J., Oorebeek, M., van Overveld, T. & Cuthill, I. C. 2005. Mutual ornamentation, age, and reproductive performance in the European starling. Behavioral Ecology 16, 805-817.

Kraaijeveld, K., Carew, P. J., Billing, T., Adcock, G. J. & Mulder, R. A. 2004b. Extra-pair paternity does not result in differential sexual selection in the mutually ornamented black swan (Cygnus atratus). Molecular Ecology 13, 1625-1633.

- ., Gregurke, J., Hall, C., Komdeur, J. & Mulder, R.A. 2004a. Mutual ornamentation, sexual selection, and social dominance in the black swan. Behavioral Ecology 15, 380-389.

Mack, A. L. & Jones, J. 2003. Low-frequency vocalizations by cassowaries Casuarius spp. The Auk 120, 1062-1068.

Ord, T. J. & Stuart-Fox, D. 2006. Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change. Journal of Evolutionary Biology 19, 797-808.

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

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

Roulin, A., Dijkstra, C., Riols, C. & Ducrest, A. L. 2001. Female- and male-specific signals of quality in the barn owl. Journal of Evolutionary Biology 14, 255-266.

South, S. H. & Arnqvist, G. 2011. Male, but not female, preference for an ornament expressed in both sexes of the polygynous mosquito Sabethes cyaneus. Animal Behaviour 81, 645-651.

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.

Tobias, J. A., Gamarra-Toledo, V., García-Olaechea, D., Pulgarín, P. C. & Seddon, N. 2011. Year-round resource defence and the evolution of male and female song in suboscine birds: social armaments are mutual ornaments. Journal of Evolutionary Biology doi: 10.1111/j.1420-9101.2011.02345.x

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

West-Eberhard, M. J. 1979. Sexual selection, social competition, and evolution. Proceedings of the American Philosophical Society 123, 222-234.

- . 1983. Sexual selection, social competition, and speciation. Quarterly Review of Biology 58, 155-183.

Widemo, M. S. 2003. Mutual mate choice in the deep snouted pipefish Syngnathus typhle. Acta Universitatis Upsaliensis. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 801. 31 pp.

Wiens, J. J. 2001. Widespread loss of sexually selected traits: how the peacock lost its spots. Trends in Ecology and Evolution 16, 517-523.

Darren Naish About the Author: Darren Naish is a science writer, technical editor and palaeozoologist (affiliated with the University of Southampton, UK). He mostly works on Cretaceous dinosaurs and pterosaurs but has an avid interest in all things tetrapod. His publications can be downloaded at darrennaish.wordpress.com. He has been blogging at Tetrapod Zoology since 2006. Check out the Tet Zoo podcast at tetzoo.com! Follow on Twitter @TetZoo.

The views expressed are those of the author and are not necessarily those of Scientific American.





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  1. 1. Dave Hone 5:43 am 01/5/2012

    Thanks for the awesome and massive write-up Darren. And yep, my original post was a bit short because I wanted to get it out with the paper and we’d just written a 60 page manuscript and I didn’t feel up to much more. For those interested I have posted a couple more on some of the details of the paper:

    See this article on crest size in theropods and this one on theropod sociality.

    Link to this
  2. 2. David Marjanović 6:17 am 01/5/2012

    the Palawan peacock-pheasant photo is by Dante Alighieri

    That’s really not likely to be his meatspace name!

    Link to this
  3. 3. Jerzy New 6:31 am 01/5/2012

    Interesting is apparent absence of extreme sexual dimorphism in ornaments of dinosaurus (like, horns of adult male ibex are several times larger than adult female, or male deer have antlers, females don’t).

    This suggests that:
    - Adult males and females are misidentified as different species,
    - Breeding system of dinosaurs was very different than many of modern ungulates.

    The latter is quite interesting when we add the fact that dinosaurs were oviparous plus likely had very long incubation period, so possibly adult males and females were kept long time to incubate/defend the brood.

    Link to this
  4. 4. Jerzy New 6:34 am 01/5/2012

    … or, adult females are misidentified as juveniles.

    HMW Vol. 2 has quite an interesting discussion on why bovids have horns in males only or in both sexes depending from size and habitat. Don’t remember details, but it might be very enlightening on dinosaur social system.

    Link to this
  5. 5. naishd 6:38 am 01/5/2012

    David: yes, you know that, I know that, he/she knows that :)

    Jerzy – I do understand that some comparisons between herbivorous dinosaurs and extant ungulates are unavoidable. But… why assume otherwise that the two were similar in social/sexual behaviour? Ungulates practise K-selection and are viviparous; Mesozoic dinosaurs seem to have been mostly r-selected, and of course they were oviparous nest-builders. I think the presence of mutual ornamentation in the dinosaurs indicates that they were doing things rather differently from the ungulates, not that (since they don’t fit neatly in an ungulate model) we’ve made a mistake in interpreting them.

    Regarding sexual dimorphism in extant ungulates, see our paper – we have some discussion of dimorphic horn morphology in bovids. I can send you the pdf.

    Darren

    Link to this
  6. 6. Jerzy New 10:20 am 01/5/2012

    @naishd
    “why assume otherwise that the two were similar in social/sexual behaviour”

    Because it is basic principle in behavioral ecology: that social system is partially shaped by environmental pressures.

    For example, modern ungulates often congregate in favorite areas like patches of good forage or waterholes. This often creates a mating system where males defend territories around such resources and mate with visiting females. Because Mesosoic landscapes were also likely patchy, then…

    So, back to topic:

    How I interpret your finding is that male dinosaurs often cooperated in parental care. For which we even have some primary proofs (skeletons of brooding dinos established to be males).

    To sum up: why females should have ornaments? Because males are selective. Why males should be selective at all? Males produce lots of sperm compared to female producing limited number of eggs or young. So why selection? Males are picky only if they themselves provide resources for young, in form of parental care.

    There may be lots of reasons why males provide parental care in amniotes. In dinos likely is the situation like in ostriches: long incubation compared with impossibility of nesting in a place inaccessible to predators means that both sexes must take turns in incubation and protecting the nest.

    Link to this
  7. 7. naishd 10:33 am 01/5/2012

    Darren says: “why assume otherwise that the two (herbivorous dinosaurs and extant ungulates) were similar in social/sexual behaviour”

    Jerzy says: Because it is basic principle in behavioral ecology: that social system is partially shaped by environmental pressures.

    Darren now says: what – - that a ‘basic principle in behavioural ecology’ is that ungulates should convergently resemble Mesozoic dinosaurs? Like I said, I’ll give you that there were similarities in some aspects of their behaviour, ecology and morphology, but the fact remains that there are many other ways to behave sociosexually. Ungulate behaviour often involves harem defence by big, showy males (with resource defence being commoner in small-bodied species) – this actually seems very different from what we know of herbivorous dinosaurs, so I’m not sure I see your point! (there are also ungulates that practise monogamy, or display via leks).

    On other points – yes, you are right about the apparent correlation between mutual ornamentation and biparental care/monogamy. But note that males are not _only_ picky “if they themselves provide resources for young” – actually, male choosiness is now known to operate across a range of species, even in species where males don’t contribute to parental care. Classic example: Great snipe Gallinago media. Why should males be choosy? Several reasons, one being that sperm is not a limitless resource.

    Darren

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  8. 8. Halbred 2:05 pm 01/5/2012

    I would love a copy of the PDF as well. It’s Zach Miller by the way–I should just re-register with that as my username.

    Interesting idea, and I’m surprised it hasn’t been brought up in the past. As to ceratopsids that lost their brow horns: this happened twice, once in centrosaurines (as a whole) and once in chasmosaurines (in the Vagaceratops lineage). Note that, in centrosaurines, the brow horns are never completely lost, just strongly reduced–in their place, the nasal horn usually gigantifies. Look at Centrosaurus, Styracosaurus, and Rubeosaurus as examples. Centrosaurines also tend to have more complicated parietal ornamentation than chasmosaurines. I’m not sure what the mechanism would be, but somewhere along the centrosaurine line, males and females must have switched from caring about postorbital horns to nasal horns and parietal spikes.

    The Triceratops group provides an interesting case study for chasmosaurines, though. Previously to the origin of this group, chasmosaurines had long brow horns and tall, showy frills. Triceratops and its close relatives (“Triceratopsini?”) went with a shorter, rounder frill with nothing but little episquamosals and epiparietals surrounding it. So, again hypothetically, somewhere along the chasmosaurine line, males and females stopped caring about frill ornamentation. The weird thing is that triceratopsines don’t have a “replacement” feature like centrosaurines do.

    And Darren, I’d love to hear your thoughts on the “Toroceratops” hypothesis.

    Link to this
  9. 9. pmurphy98 2:48 pm 01/5/2012

    Excellent article! One of my favorites in a long time!

    And I’m far from a reliable source, but isn’t the “_Pteranodon_” in the diagram towards the top now called _Geosternbergia_?

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  10. 10. jtdwyer 3:37 pm 01/5/2012

    I can’t assess the assertions made in this article, but it’s certainly interesting – thanks!

    One comment about pterosaurs’ crests: while they may have developed primarily for display purposes, they would also have had to be aerodynamically functional to some minimal extent or flight capabilities would have been negatively impacted.

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  11. 11. naishd 3:51 pm 01/5/2012

    Thanks for comments. To those currently having problems registering and thus being barred from leaving comments – this is a known problem that sometimes affects me as well. Sorry, nothing I can do except pass the message on.

    Zach: yes, brow horns were strongly reduced at least twice in ceratopsids. You’re not quite right about centrosaurines: the horns are indeed completely lost in some (e.g., Styracosaurus and Pachyrhinosaurus), being resorbed and replaced by ovoid depressions. It used to be thought that small hornlets sat inside these depressions but… nope. And the same thing happened in some chasmosaurines: Chasmosaurus irvinensis and some indeterminate Chasmosaurus specimens have those depressions as well.

    Epoccipital loss in the Triceratops lineage: it might not be that epoccipital loss somehow reflects the fact that the animals stopped using frill-edge ornaments in display; rather, it might be that ornament loss represents (paradoxically) a new form of ornamentation. As I discussed with respect to swordtails and so on above, selection may have acted upon loss of the respective ornamentation, perhaps because it was this loss that made the taxon distinct from its relatives. I’m speculating, but I don’t think this is an unreasonable interpretation.

    As for Horner’s ‘unified frame of reference’ hypothesis (aka ‘ontogenetic morphing’/'Toroceratops’), I certainly don’t have a problem with it in principle and think that it’s pretty reasonable based on some of the ontogenetic changes we see in living taxa (and based on the histological data that the respective authors have presented). But – - I wish its proponents would do a better job of stating that it’s a hypothesis, and as yet not a widely accepted one. No, nobody has “shown” that Triceratops grows into Torosaurus at some specific point in ontogeny (nor has it been “shown” that Dracorex and Stygimoloch both turn into Pachycephalosaurus) – rather, the idea has been presented that this might happen. It might happen. But it might not. Or, it might happen for some of the taxa mentioned and not others. I am now convinced that Nanotyrannus is not Tyrannosaurus, and I still think Torosaurus is a taxon, not a growth stage. But I’m not a ceratopsian worker, and I wait for my colleagues in that field to publish more on this issue.

    Darren

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  12. 12. Dave Hone 4:43 pm 01/5/2012

    @jtdwyer Actually that is what you would expect to a degree. A negative impact on flight capability would therefore be a very strong and honest signal of fitness. If you can survive while lugging that thing around on your head you must be doing something right. Actually some work has suggested these had surprisingly little effect, but even if they were strongly negative that still fits with them being sociosexual siganls (as indeed are the curled primary feathers of the black swans mentioned above).

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  13. 13. Dave@reptileevolution.com 5:25 pm 01/5/2012

    Darren,

    I fully agree with your concept.

    However, why did you reference and support Bennett (1992, 1994) and Lu et al. (2011) promoting sexual dimorphism? It doesn’t support your hypothesis.

    Then you referenced adolescent development of a bony crest in thalassodromids (Martill and Naish 2006), but this example indicates that crests developed long before half adult size had been reached and therefore precedes interest in sex. Contra the tack you were taking, >thatcould< all be male, but the odds are stacked against that.

    There's more in pterosaurheresies.com, Dec. 25, 2010.

    Just curious about your example choices.

    Dave

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  14. 14. naishd 5:34 pm 01/5/2012

    Dave (comment 13): you misunderstood. Pteranodon and Darwinopterus were discussed because I wanted to say that some crested pterosaurs seemingly display sexual dimorphism: that is, these dimorphic taxa are NOT the ones that appear to be candidates for mutual sexual selection. For MSS to be in play, we would predict that males are females exhibit similarly elaborate ornamentation (possible example: Dsungaripterus). This should all be clear from the text. In other words, I’m just noting that sexual dimorphism where males were the showy ones AND mutual sexual selection were perhaps present in different pterosaur lineages. Nothing problematic or contradictory about this based on what we know of living animals.

    The thalassodromid with the incipient crest is best interpreted as a juvenile, just starting to grow a crest that will be ‘subadult’ or ‘adult’ in form by the time the animal is sexually mature. As I said in the article (in connection with ceratopsians), sexual display structures have to start growing at some time.

    I hope this clears things up. Let me know if not.

    Darren

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  15. 15. Halbred 6:52 pm 01/5/2012

    Ah yes, the pits. I don’t know if I’d discount my beloved Pachyrhinosaurus from having postorbitals. Juveniles have small postorbital horns, and they “blossom” into big bosses. They’re not horns, but they are…postorbital somethings.

    I was wrong about Styracosaurus–I thought it retained very small postorbital horns, but a quick look at the redescription shows it does not! One more thing, Vagaceratops = Chasmosaurus irvinensis.

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  16. 16. naishd 7:06 pm 01/5/2012

    Oh yeah, sorry, Chasmosaurus irvinensis = Vagaceratops, I forgot.

    On a similar note, yes, Pteranodon sternbergi is indeed Geosternbergia (comment 9). I don’t agree with all of the recent taxonomic changes proposed for pteranodontids, but that one looks pretty reasonable.

    Darren

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  17. 17. Tamara Henson 8:14 pm 01/5/2012

    I agree with you 100% on both ‘digital publication’ should be synonymous with ‘publication’ and Horner’s hypothesis. I have actually been trolled online for stating that it is a hypothesis and not a fact. The idea has a lot of holes in it (pun intended)including the fact while Triceratops horridus and Torosaurus latus overlapped in range Triceratops prorsus and Torosaurus (or whatever taxon it will eventually be assigned to)utahensis did not.

    The thing that annoys me the most is that most arguments on the web for this idea are along the lines of ‘two elephant-sized animals with similar morphology cannot live in the same area’. Ummm Ok, what about Africa where there are two species of elephants that occasionally overlap in range? Sigh, I wish the dino-fanboys would look at living animals for a change.

    “I am now convinced that Nanotyrannus is not Tyrannosaurus” Now this is a subject that interests me. Where can I find this new study that disputes the seemingly universal ‘nano is a baby rex’ idea?

    Sorry I haven’t been commenting lately. Scientific America is a real pain to log in on (it often jumps me to a different blog when I log in)so i just haven’t bothered. Rest assured I always read your posts Darren.

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  18. 18. validnano 8:37 pm 01/5/2012

    Tamara Henson Nanotyrannus is definitely distinct and valid.A new specimen from Montana shows this, completely different from T.rex and others with much longer hand, longer neck and other differences.The skeleton is presrved ontop of a new ceratopsian. You can see a video of both specimens here on youtube http://www.youtube.com/watch?v=rkjTdiIVH8s or can google dueling dinosaurs to see much more.

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  19. 19. JAHeadden 9:01 pm 01/5/2012

    Zamyn Khondt oviraptorid (often incorrectly labeled Oviraptor)

    Whoever wrote that line, thank you for that!

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  20. 20. vdinets 10:00 pm 01/5/2012

    My understanding is that deer antlers also function as endocrine glands of sort, as long as they are in velvet stage.

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  21. 21. falcon121 10:41 pm 01/5/2012

    Can I have a copy of the PDF as well please?

    Does MSS explain why monogamy is so common in birds?

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  22. 22. JennDeland 11:43 pm 01/5/2012

    Online is not publication, because online is ephemeral, while dead trees last. I remember a time before there was an internet. (All right, I guess I’m a little older than you, Darren, but not geriatric yet.) Your children may well see something you would not recognize. When you cite something, you want to be referring to something that will still exist when your words are being read.

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  23. 23. Therizinosaurus 12:58 am 01/6/2012

    Very interesting. I didn’t even know MSS existed as some sort of common strategy. “Furthermore, cranial ornaments in living species don’t – so far as we know at the moment – work as ‘species identifiers’ (Knell & Sampson 2011)” reinforces my belief that most of what paleontologists say about behavior and function is pulled out of their ass (in this case that crests work as species identifiers) and we desperately need studies of living taxa before we can say much about extinct ones.

    About the only thing I can contribute is that “theropod crests appear at Avepoda and stop at Coelurosauria” really doesn’t seem to be the actual trend. While coelophysoids might be basally crested, only Ceratosaurus and a few abelisaurids have crests in Ceratosauria. Taxa like Limusaurus, Masiakasaurus, Abelisaurus, Aucasaurus, Skorpiovenator and Rugops break that up to make it more parsimonious the clade began crestless. Among all non-carnosaur, non-megalosaur tetanurines, only Monolophosaurus even preserves the area, so that’s a terrible sample size. In Megalosauroidea, megalosaurids lacks crests even if you count the little nasal cone of spinosaurids. In carnosaurs, only Allosaurus has anything tall enough to really count. In Coelurosauria, besides oviraptorids, there’s also proceratosaurids and CM 78000/78001. Besides, with Tianyulong and the new feathered baby megalosaur (=Juravenator?), evidence is better all the time that feathers date back to the base of Dinosauria or Ornithodira anyway.

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  24. 24. Therizinosaurus 1:30 am 01/6/2012

    Not really on topic, but I want to be sure people don’t take “validnano”‘s proclaimations of the definite validity of Nanotyrannus as truth. The new spcimen looks interesting, but it’s not even mentioned in the technical literature yet. The differences they note (better developed semilunate and humeral external tuber, longer neck, shallow coracoid) are plesiomorphic for tyrannosaurs, so are expected in juveniles. Note Shanshanosaurus has a much longer neck and shallower coracoid than Tarbosaurus, its probable adult form. The different gastralia are too vague to comment on, as with the furcula (though it varies a lot in Tyrannosaurus individuals). The video’s full of hyperbole (don’t get me started on their behavioral ideas), like saying Nanotyrannus is in a separate subfamily from Tyrannosaurus, which is complete crap. Finally, every supposed Nanotyrannus found makes it more curious why no actual juvenile Tyrannosaurus are preserved. There are rumored small Tyrannosaurus teeth, but these never manage to get published…

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  25. 25. Andreas Johansson 7:53 am 01/6/2012

    Tangentially, wrt #23, could someone point me to a decent overview of non-coelurosaurian theropod relationships? I lose track of where megalosaurs and abelisaurids and whatnot are supposed to be nowadays.

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  26. 26. BilBy 7:55 am 01/6/2012

    Darren – another request for the pdf as well please. Excellent post, thanks.

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  27. 27. Jerzy New 8:25 am 01/6/2012

    @naishd
    Great snipe is extreme example of male choosiness, but note that females there don’t have ornaments.

    Some thoughts:
    The case for mutual sexual selection seems strongest in carnivores (Ceratosaurus, Carnotaurus, Dilophosaurus etc). They had sharp teeth which presumably were more effective in within-sex status disputes, so social selectioncan be refuted.

    Some dinosaur ornaments so closely resemble ungulates (Triecratops horns – wild cattle and yak, pachycepholosaurs – sheep, Amargasaurs – oryx/gemsbok) that it is really difficult to argue they were not used for social dominance and predator fighting.

    Difficult is to reconcile crests in pterosaurs with the idea that pterosaurs flew as hatchlings and supposedly received no parental care. So what would sexes compete for? I guess you had two strategies of pterosaurs – with parental care and crests, or without and with no ornaments or sexual dimorphism.

    Crests of pterosaurs, could be a good argument that many of them spend little time flying, contra reconstruction as albatross-like pelagic fish-eaters. Tapejarids as clambering forest canopy dwellers, Nyctosaurus as perch-hunting kingfisher analogue, perhaps?

    Still, there is exciting topic for paleontologists with access to primary material of more abundant dinosaurs – checking if ornaments correlated with sex of the fossils, and if individuals without preserved ornaments really missed them and if they could or couldn’t be juveniles.

    BTW – anybody looked if there are objective marks of immaturity/full growth in dinosaurs and pteroasurs, like some not completely ossified bones in juvenile mammals?

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  28. 28. naishd 9:25 am 01/6/2012

    Thanks for all the comments. I’m not going to be able to keep up with responses. But, in response to Mickey (comment 23)…

    ———————-
    About the only thing I can contribute is that “theropod crests appear at Avepoda and stop at Coelurosauria” really doesn’t seem to be the actual trend. While coelophysoids might be basally crested, only Ceratosaurus and a few abelisaurids have crests in Ceratosauria. Taxa like Limusaurus, Masiakasaurus, Abelisaurus, Aucasaurus, Skorpiovenator and Rugops break that up to make it more parsimonious the clade began crestless. Among all non-carnosaur, non-megalosaur tetanurines, only Monolophosaurus even preserves the area, so that’s a terrible sample size. In Megalosauroidea, megalosaurids lacks crests even if you count the little nasal cone of spinosaurids. In carnosaurs, only Allosaurus has anything tall enough to really count. In Coelurosauria, besides oviraptorids, there’s also proceratosaurids and CM 78000/78001. Besides, with Tianyulong and the new feathered baby megalosaur (=Juravenator?), evidence is better all the time that feathers date back to the base of Dinosauria or Ornithodira anyway.
    ———————-

    Firstly, note that we pose this idea as a question: “Did feathers replace crests in coelurosaurian theropods?” (p. 12)… so, it’s a suggestion. Secondly, it might only apply to complex feathers, not to stage 1 filaments. Thirdly, cranial ornaments are more widespread in theropods than you state: if that is, the term ‘cranial ornamentation’ is taken to apply to the excrescences, bumps, hornlets, ridges and so on that look like they might have served a role in visual display, and not just to extravagant dilophosaur- or ceratosaurid-style plates or horns. So, ornaments are widely present in abelisaurs (even seemingly unornamented taxa, like Skorpiovenator, have weird ‘inflated’, strangely textured regions on the dorsal part of the postorbital), preorbital hornlets are present in megalosauroids like Afrovenator, and preorbital hornlets and nasal ridges are present throughout Allosauroidea. The idea may or may not hold up – I’m not especially attached to it (it’s Dave’s idea, not mine).

    Darren

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  29. 29. Dave Hone 9:58 am 01/6/2012

    Just to add into that, as I noted on the Musings there are good reasons to think that theropods would have had considerably smaller crests than ornithischians, even if both were doing the same thing (signalling to conspecifics) and so yes, I’m quite happy with even quite minor bosses etc. on theropods being considered crests that could be used in display.

    As Darren says, this is a hypothesis. Obviously it needs testing, but I think it has merit and it hadn’t been suggested before, despite discussions of crests and feathers being used for siganlling. If both were then it would make sense that you don’t *necessarily* need both, and that feathers might well have the edge (can be erected, provide other functions, can be shed / seasonal colours etc.).

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  30. 30. naishd 10:05 am 01/6/2012

    Unsurprisingly, this article is now top of the list in the ‘most commented posts’ list (“unsurprising” because the registration and logging-in system means that SciAm blogs receive but a fraction of the commenting that they should – hey, change is in motion). But the softshell turtle article is still the only one in the ‘most read posts’, go figure.

    Darren

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  31. 31. David Marjanović 10:47 am 01/6/2012

    [nonavian] dinosaurs were oviparous plus likely had very long incubation period

    Why do you think they had a long incubation period? Those eggs were small.

    Mesosoic landscapes were also likely patchy

    The Morrison Formation isn’t the entire Mesozoic.

    No, nobody has “shown” that Triceratops grows into Torosaurus at some specific point in ontogeny (nor has it been “shown” that Dracorex and Stygimoloch both turn into Pachycephalosaurus) – rather, the idea has been presented that this might happen.

    Erm, no. The following has been shown:

    – All investigated Triceratops specimens are histologically immature.
    – All investigated Torosaurus specimens are histologically mature.
    – There are intermediate specimens with conspicuous thinnings in the frill, and others with small circular fenestrae. I’m not counting Nedoceratops (formerly Diceratops) simply because I haven’t read the paper or seen the photos.
    – Adults are expected to be rarer than immature individuals.
    Triceratops is already known to undergo a lot of ontogenetic transformation: the epoccipitals flatten, and the horns reverse curvature, which requires bone resorption. Growing holes in the frill doesn’t sound outrageous.
    – I don’t remember the details that Scannella and Fowler presented in their Romer Prize talks in 2010, but they say their high-resolution stratigraphy and stuff resolves all the problems of Triceratops horridus/prorsus and Torosaurus latus/utahensis.
    Dracorex is histologically juvenile, with a fast-growing skull.
    Stygimoloch has a growing dome, while the spikes are being resorbed.
    Pachycephalosaurus is histologically adult.

    I don’t know why pachycephalosaurs would grow long spikes and then resorb them while growing up. But that’s what Stygimoloch did. I can’t help it. Published together with Dracorex and Pachycephalosaurus in the Festschrift for Armand de Ricqlès in Comptes Rendus Palevol.

    Very interesting. I didn’t even know MSS existed as some sort of common strategy.

    Brains in humans? Aren’t those a likely example?

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  32. 32. John Harshman 1:23 pm 01/6/2012

    Hey, I can log in now! Someone asks if MSS explains monogamy in birds. Not really. But high male parental investment explains both MSS and monogamy. There is competition for limited resources. In most species, eggs are a limiting resource, and so there is competition among males for females and choosiness among females for males. Male gametes are not very limited, so in species where males contribute only gametes, there is no competition among females for males or choosiness among males, who are glad to provide sperm to anyone. But male parental care is another limited resource, and so in species where males do a lot of this there is competition among females for male partners and so choosiness among males. Thus some signal of female quality may arise through sexual selection.

    Note that social monogamy in birds may conceal a great deal of genetic polygamy. It’s a complicated story. The best females may get the best male social mate. Less able females may get less desirable social mates, but may solicit genes from the best male, who is glad to oblige. Everybody wins. The best male gets lots of offspring. The best female gets all her eggs fertilized by the best male. Lesser females get some quality offspring from the best male and some parental care from their social mates. Lesser males get some paternity in return for parental care. And those are only a few of the complications.

    How you would show any of this in extinct theropods is unclear. By the way, it seems to me that only stage III feathers, with large, flat surfaces like those of Caudipteryx, would be very useful in sexual display.

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  33. 33. David Marjanović 2:34 pm 01/6/2012

    Brains in humans? Aren’t those a likely example?

    …and while I was clicking on “Submit Comment”, I remembered that I’ve read that Darwin proposed exactly this in his abovementioned 1871 book.

    The case for mutual sexual selection seems strongest in carnivores (Ceratosaurus, Carnotaurus, Dilophosaurus etc). They had sharp teeth which presumably were more effective in within-sex status disputes, so social selectioncan be refuted.

    Don’t such dangerous weapons provide rather strong selection pressure for not using them?

    Difficult is to reconcile crests in pterosaurs with the idea that pterosaurs flew as hatchlings and supposedly received no parental care. So what would sexes compete for?

    Parental care isn’t the only parental investment!

    Crests of pterosaurs, could be a good argument that many of them spend little time flying, contra reconstruction as albatross-like pelagic fish-eaters. Tapejarids as clambering forest canopy dwellers, Nyctosaurus as perch-hunting kingfisher analogue, perhaps?

    You overlook the size and, well, the anatomy of these animals. Nyctosaurus as a percher? What have you smoked, and can I get it legally in the Netherlands?

    Still, there is exciting topic for paleontologists with access to primary material of more abundant dinosaurs – checking if ornaments correlated with sex of the fossils

    And how do you propose to determine their sexes? Usually, the only available method is to find an egg or two inside the birth canal. Pelvis width differences like in Pteranodon are rare outside of placental mammals.

    BTW – anybody looked if there are objective marks of immaturity/full growth in dinosaurs and pteroasurs, like some not completely ossified bones in juvenile mammals?

    Sure. Bone histology, fusion of the suture between the centrum and the neural arch of each vertebra (which doesn’t happen at the same time everywhere in the vertebral column, BTW)… though, in terrestrial ones, that’s pretty much it. Separate ossification centers in the epiphyses are limited to mammals, squamates, and the tibia of crown-group birds, IIRC.

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  34. 34. Dave Hone 3:00 pm 01/6/2012

    “Still, there is exciting topic for paleontologists with access to primary material of more abundant dinosaurs – checking if ornaments correlated with sex of the fossils”

    But if, as we argue, mutual sexual selection is ongoing and, as noted in a number of places for some species we have dozens of fossils with no / very weak dimorphism, how do you tell them apart? If both males and females are ornamented and those ornaments are similar in form and size and the rest of the anatomy is comparable, how do you pick them apart?

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  35. 35. John Harshman 5:37 pm 01/6/2012

    The presence of medullary bone might be a test for sex. Unfortunately, while presence diagnoses a female, absence diagnoses either a male or a female not getting ready to lay eggs.

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  36. 36. Therizinosaurus 7:56 pm 01/6/2012

    Fair enough that it’s Hone’s idea. If we’re counting even small structures, lacrimal horns last through tyrannosauroids and the taxa that might be basal tyrannosauroids or slightly closer to birds (e.g. Tanycolagreus), but are also in Pelecanimimus. Nasal ridges last a bit further, being seen not only in things like Dilong, but also compsognathids. Nasal rugosities are present in most tyrannosauroids, but also some ornithomimids. Most maniraptoriforms don’t have lacrimal horns, but many do have laterally projecting processes in the same position. Were these visible in the living animal? In any case, if you did some statistical test for cranial ornamentation prominence in theropods, I think body size would be at least as well correlated as stage III feathers.

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  37. 37. Maija Karala 5:22 am 01/7/2012

    “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?”

    How likely is it that we simply can’t recognize very closely related species because they lack soft tissues/dna/sufficient sample size, or simply were never found?

    I’m not an expert in any sort of osteology, but I doubt there woukd be any way to discriminate between, say, the 70-or-so species in the genus Phylloscopus based only on more or less (mostly less) complete fossilized bones.

    Well, that might be an extreme example. But my point is that there might have been groups of very similar, closely related species that recognized each other by things other than differences in bony structures. Colors, ornamental scales, vocalizations?

    What this has to do with cranial crests is that even if these species had an identical crest, it could have been used in species recognition devices by simply being a different color. Differences in details are just as useful, and easier to evolve, than fundamentally different ornaments.

    Of course, there’s basically no way to test this (or is there?). It’s just useless speculation. As a paleoartist, I would be interested to know if it’s completely inplausible to draw, say, three very similar, but differently colored species of Microraptor coexisting.

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  38. 38. Dave Hone 5:33 am 01/7/2012

    Several things in that last comment, and I’ll try to brief as much of it is in the paper.

    We do have a big go at the species recognition hypothesis (as indeed have others before us). You can recognise a conspecific by colour, pattern, behaviour, calls, breeding season etc. etc. why grow and carry 50 lbs of bone just to do that? One can have a red head and one a blue head whether they have a frill and spikes or not. Plus lots of other animals have no trouble with recognising conspseicifcs that look similar, and in plenty of cases these animals lived more or less alone.

    I agree that there are probably cryptic species in the fossil record that can’t be told apart on osteology alone. I doubt you could tell a Grevy’s zebra from a Chapmans or even a quagga on osteology alone from a small sample size. But I think that’s a separate issue to the one here, you’d expect crests as we infer them to be different in each species as they’re under a different kind of selection pressure.

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  39. 39. naishd 7:55 am 01/7/2012

    Some responses…

    Jerzy (comment 27) said that “The case for mutual sexual selection seems strongest in carnivores (Ceratosaurus, Carnotaurus, Dilophosaurus etc)”. The difference here is perhaps between the theoretical case as you imagine it, and the case that we (mostly) present based on specimens. So, MSS is mostly stated by us to apply to such groups as lambeosaurines, ceratopsids and pterodactyloids because this is where sample size demonstrates a similar degree of ornamentation in both males and females. Sample sizes are not good enough to establish this for all the theropods you mention – they might exhibit strong sexual dimorphism in ornamentation for all we know (though, yes, we do suggest that Ceratosaurus might represent a possible case of MSS).

    Pterosaurs: I can agree that the crests look stupid for perpetually flying animals, but there’s no reason to think that the taxa concerned were poor fliers, or flightless – all evidence is to the contrary. Studies indicate that they could fly just fine, even with those incredible crests.

    Jerzy also said “Difficult is to reconcile crests in pterosaurs with the idea that pterosaurs flew as hatchlings and supposedly received no parental care”. I think I see your logic: you’re saying that adults would only advertise themselves as good potential mates if the thing they were advertising was their parental abilities. But, no. Post-hatching parental care is not the only thing you want to advertise, even if you are monogamous. Potentially, there’s territory defence, nest-building abilities, egg defence – and advertising good genes in any case isn’t a bad thing.

    David M (comment 31): yes, like I said in comment 11, it may be that the proposed ontogenetic morphing occurs in some of the respective taxa, but not in others. The pachycephalosaur sequence seems least problematic: it seems that the domes were growing under strong positive allometry while the horns and spikes were increasing isometrically, or not increasing in size at all (similar spike growth is seen in some extant reptiles). While some interesting histological data has been presented for the ceratopsids, there are still several issues that require clearing up. I remain sceptical, and this isn’t because I haven’t read the papers.

    Therizinosaurus (comment 36): the points about the overlap between the presence of stage 1 feathers and tyrannosauroid-style bosses, hornlets etc. is made in the paper. The ‘bony crests vs feathers’ thing obviously isn’t absolute (again, as we note in the paper), but there still might be something in it – that is, bony crests might genuinely be rarer in feathered lineages.

    Maija Karala (comment 37): as Dave said, cryptic species – that is, those that are near-indistinguishable or indistinguishable based on osteology – likely existed in Mesozoic animals. In extant animals, close relatives can be so similar skeletally that the degree of difference that allows them to be separated can be swamped by the amount of variation seen in individuals of another, related species (in other words, A and B can be separated, but C possesses the characters seen in A and B!). These problems can only be examined when you have huge sample sizes and lots of ancillary data, so anybody who works on animals older than those from the Pleistocene basically has to ignore this area and pretend it doesn’t exist. We have to assume that the species we recognise – they’re unashamed ‘morphospecies’ only – operated as biological populations. I have to say that the cryptic species issue isn’t much of an obvious problem for our MSS proposal, since the taxa that might exhibit MSS are generally represented by closely associated specimens (e.g., ceratopsians from bonebeds, pterodactyloids from the same, coeval beds) that don’t look like potential separate species.

    Darren

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  40. 40. JAHeadden 6:10 pm 01/7/2012

    To Mickey at 36:

    Most maniraptoriforms don’t have lacrimal horns, but many do have laterally projecting processes in the same position. Were these visible in the living animal?

    I should hope not. Data with modern animals, especially lizards and birds, imply that there are the anterior limits of the supraorbital structures that form the nonbony orbital margin, and are connected to the postorbital directly. They shouldn’t define any structure bulging out from the lateral and dorsal surfaces of the skull.

    On a side note, I do not think dismissal of the issue of cranial crests exclusive of feathers is very viable, and while this can be extended simply by invoking oviraptorosaurs, it may be far too premature to presume the feathers vs. crests are mutually exclusive with some exceptions. We simply do not have data to assess the variation of integument in coelurosaurs, and it becomes trickier if you consider that some “coelurosaurs” may not actually be coelurosaurs, despite preserving “stage 1 feathers,” as in Sinosauropteryx prima. The integument may extend to much more basal taxa, including into basal theropods, and saurischians, and so forth. This is firmly enforced by the presence of “stage 1 feather”-like structures in Tianyulong confuciusi and their extension to basal ceratopsians with whatever species of Psittacosaurus SMF R 4970 belongs to. This doesn’t take into account what colored or modified skin may have to do with the situation, replacing bony or feathered crests, as in jungle fowl. The recovery of color in skin may be quite a bit harder to to achieve than color in feathers.

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  41. 41. ChasCPeterson 2:17 pm 01/8/2012

    Late to this one, but I have enjoyed the interesting post and comments.

    I note the apparent synonymization of ‘sexual selection’ and ‘mate choice’ throughout. This is of course only half of the concept, ‘intersexual selection’ in the behavioral ecology jargon. The other half is intrasexual selection: direct competition among (usually) males for access to mates. The difference is acknowledged in the literature by the categorization of secondary sexual characteristics as ‘ornaments’ or ‘armaments’ (with the realization that these functions are not mutually exclusive; google-scholar link).

    Perhaps, then, the evolution of apparent armaments like the horns and shields of ceratopsians require different explanations from apparent ornaments like pterosaur crests or colored feathers.

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  42. 42. Dave Hone 2:51 pm 01/8/2012

    Well do cover all sides of things in the paper wrt inter and intersexual selection and mate choice vs social dominance. We also break the taxa down (i.e. we don’t consider ceratopsians with pterosaurs) and even distinguish between things like the Triceratops frill vs horns. It’s (as far as possible given the restrcitions of the journal) all in there.

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  43. 43. naishd 3:27 pm 01/8/2012

    ChasCPeterson (comment 41): if there is any confusion in the article between ‘sexual selection’ and ‘mate choice’, I think I have to say that it isn’t deliberate. Actually, I’m not sure that there is confusion, since I didn’t write about the meaning of those specific terms in the article, and even made a point of citing some of the ‘ornaments vs armaments’ literature (see citation of Tobias et al. (2011) above). Furthermore, there is a reference to intrasexual competition in my text (I made the point that, in some/many taxa, it occurs in females as well as males). As Dave notes, we allude to all of this in the paper anyway.

    You do, of course, have a valid point in noting that the structures seen in the various fossil groups may well _not_ have operated under the same selective pressure.

    Darren

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  44. 44. Jerzy New 4:31 am 01/9/2012

    @naishd
    Pterosaurs flying
    I think there is a confusion here – I there are birds which can afford ornaments because they fly short distances and slow (hornbills and similar birds of forest canopy) or hunt from perches and fly fast but rarely (kingfishers). At the same time they are neither poor fliers nor good terrestrial walkers.

    “Post-hatching parental care is not the only thing you want to advertise, even if you are monogamous. Potentially, there’s territory defence, nest-building abilities, egg defence – and advertising good genes in any case isn’t a bad thing. ”

    Again, very difficult to reconcile with the vision of pterosaurs laying thin-shelled eggs (they should be incubated in nesting mounds, so hartd to see a limiting factor which would force male to limit a number of females he has).

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  45. 45. naishd 4:48 am 01/9/2012

    1. You’re making assumptions again – please explain why the crazy-crested pterosaurs were similar in flight habits to the hornbills and kingfishers you have in mind. They weren’t (though I do think that some crested pterosaurs – tapejarids – may have been somewhat similar to hornbills in _some_ aspects of biology).

    2. On link between elaborate mutual ornamentation and biparental care etc., you say “[V]ery difficult to reconcile with the vision of pterosaurs laying thin-shelled eggs”. Why? (I’m not saying pterosaurs necessarily did practise biparental care, just curious about your logic).

    Darren

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  46. 46. Dartian 6:36 am 01/9/2012

    Darren (OP):
    Cranial ornaments aren’t entirely absent in feathered theropods (oviraptorids, cassowaries, guans, curassows, helmeted guineafowl and so on)

    Exactly how many times have such cranial ornaments evolved in extant avian lineages? Do you have a list of bird species that possess them? (I can think of Casuarius, Pauxi, Mitu, Oreophasis, Macrocephalon, Numida, and the hornbills; are there others?)

    Also, given that you explicitly note that there are a few birds that possess such cranial ornaments, why did you not indicate that with an asterisk in Figs. 1 and 6 in your paper?

    David M.:
    Adults are expected to be rarer than immature individuals.

    Hmm. Are you sure about that? Were immature dinosaurs really more (or even equally) likely to be preserved in the fossil record than adult individuals were?

    Dave H.:
    I doubt you could tell a Grevy’s zebra from a Chapmans or even a quagga on osteology alone from a small sample size.

    I see the general point you’re making, but, for the record, I’d like to point out that (unless your sample size really is pathetically tiny and incomplete) you can tell a Grevy’s zebra apart osteologically from other zebras. It’s admittedly not quite as easy as one might perhaps expect, however.

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  47. 47. David Marjanović 6:38 am 01/9/2012

    The pachycephalosaur sequence seems least problematic: it seems that the domes were growing under strong positive allometry while the horns and spikes were increasing isometrically, or not increasing in size at all (similar spike growth is seen in some extant reptiles).

    Fun is, it’s crazier than that. The spikes in Stygimoloch aren’t merely not growing, they’re being actively resorbed.

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  48. 48. David Marjanović 6:43 am 01/9/2012

    David M.:
    “Adults are expected to be rarer than immature individuals.”

    Hmm. Are you sure about that? Were immature dinosaurs really more (or even equally) likely to be preserved in the fossil record than adult individuals were?

    1) Most known Mesozoic dinosaurs were subadult according to things like the amount of fusion between centra and neural arches;
    2) in the cases where we know anything about their reproduction, they laid lots of eggs and look like classic r-strategists.

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  49. 49. Dartian 6:52 am 01/9/2012

    David:
    Most known Mesozoic dinosaurs were subadult

    Wow, interesting. And slightly counterintuitive.

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  50. 50. Dave Hone 7:45 am 01/9/2012

    “Dave H.:
    “I doubt you could tell a Grevy’s zebra from a Chapmans or even a quagga on osteology alone from a small sample size.”

    I see the general point you’re making, but, for the record, I’d like to point out that (unless your sample size really is pathetically tiny and incomplete) you can tell a Grevy’s zebra apart osteologically from other zebras. It’s admittedly not quite as easy as one might perhaps expect, however.”

    Interesting. It was only supposed to be a hypothetical example, I’ve not looked at the actual skeletals. Though don’t forget that for a lot of Mesozoic dinosaurs we do only have a couple of incomplete skeletons for each of several putative species – sample sizes can be very small.

    “Also, given that you explicitly note that there are a few birds that possess such cranial ornaments, why did you not indicate that with an asterisk in Figs. 1 and 6 in your paper?”

    We realised too late to change we’d forgotten to do that. But as it was mentioned in the text it’s a pretty minor issue / error.

    More generally wrt all the bird / crest / feathers stuff, this is (at the moment) just us advocating a hypothesis. Yes to test it we need to look at what might count or not as a crest and cross reference *that* with whether or not it might have had a signalling function, and do the same for feather structures (like the Caudipteryx tail fan) and cross reference all that with something like a species level phylogeny of theropods and basal birds.

    In short, massively beyond the scope of the paper as it was. However, among all the discussion of feather origins and crest function, no one had made a connection between the two, despite many advocates for each being used primarily for signalling. We think it is *plausible* that there is one, we have a bit of evidence which suggests it might be correct, and we can provide some additional minor support as to why it could work in terms of evolutionary pressures. Basically we think it’s a valid and new hypothesis ripe for testing, so we put it out there and discuss it a bit. That’s more or less it for now.

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  51. 51. Dave Unwin 9:33 am 01/9/2012

    Excellent post on an important paper. The idea that sexual selection requires sexual dimorphism, and thus can only be identified in fossils on the basis of dimorphism, grossly distorts a complex phenomenon and has seriously impeded our understanding of sexual selection in vertebrates. As Hone et al. 2011 make clear, mutual sexual selection, in its purest form (where the same ornamentation occurs in both genders), or as an imperfect dimorphism (with perfect dimorphism, at the other end of the scale, defined as presence/absence), could help to explain many of the oddities of the fossil record. Pterosaurs, and in particular Pteranodon, provide a good example.

    There are six species of pterosaur in which perfect dimorphism of cranial crests can be demonstrated. These include Darwinopterus where gender can also be confidently assigned: crested individuals = males, crestless = females. In addition there are a further 12 candidate cases of dimorphism based on crest presence/absence. By contrast, the crania of P. longiceps (of which there are more than 50 examples – see Bennett 1991) always bear a crest. Bennett (1992) has shown that the smaller morph, interpreted as female, bears a relatively small crest, whereas the larger, presumably male, morph has a relatively large crest. This interpretation has become widely accepted, but raises the issue of the function of the cranial crest in females. Bennett clearly favoured genetic correlation “the small crests of females then may be a consequence of the development of large crests in males”. Hone et al. 2011 provide an alternative and seemingly somewhat more attractive explanation, that the crests of females were also used for display. Moreover, the nice thing about this explanation is that it still works for Pteranodon even if one rejects the idea of dimorphism in relative crest size and simply assumes that there is a single ontogenetic series in which both sexes are present (since it seems extremely unlikely that only a single gender is preserved), but cannot be discriminated from one another (I don’t think this is the case, but it’s a useful thought experiment). If the latter is true this would qualify as a case of perfect MSS, rather than imperfect MSS as it seems at present.

    In my view Pteranodon is by far and away the best candidate for MSS in pterosaurs. There are around five other species of pterosaur, represented by at least four or five individuals, in which all the crania found so far bear crests (most prominently: Dsungaripterus, Tapejara and Tupuxuara). These might also be considered candidate cases for MSS, but the number of specimens involved is a magnitude less than in Pteranodon and there is still a real possibility that ‘crestless’ variants might be found – indeed, such already appears to be the case for Tupuxuara, but I’ll say no more about this for now. Even if future finds firm up the argument for MSS in all these candidate cases, its incidence in pterosaurs (present, at best, in <5% of all known species; or <12% of all species in which crests are expressed) is still very low and thus one might ask to what extent was MSS of any real significance to the behaviour, reproductive biology or evolution of pterosaurs?

    That said, I am sure that everyone would agree that having MSS in the frame is a good thing (well, ok, nearly everyone). The challenge now is to devise practical approaches that might help us to discriminate between MSS and other potential explanations (e.g. genetic correlation, species recognition, weird taphonomy) for the patterns of crest distribution that we see in the fossil record. Returning to Pteranodon – species recognition and weird taphonomy can be safely rejected, but supposing for a moment that the interpretation of sexual dimorphism is incorrect and that the crests of males and females were the same. How then might we distinguish MSS from genetic correlation? I suppose one might argue that, all other things being equal, MSS is more likely to result in this particular pattern of crest distribution, but its not a very strong argument. However, if we go with the prevailing opinion for Pteranodon – imperfect dimorphism, things become even more difficult since there does not appear to be any obvious reason to prefer MSS over genetic correlation.

    For pterosaurs, at least, this might not be so bad. If my prediction regarding the incidence of MSS in this group is anywhere near correct then, even if effective tests for MSS cannot be devised, this should not unduly hamper research on this group. Moreover, the clear cut examples of crest dimorphism in, for example, Darwinopterus (where to our great good fortune gender can also be assigned), means that we will be able to make progress in understanding sexual selection in pterosaurs irrespective of how tractable (or intractable) MSS proves to be.

    On the other hand, the situation in dinosaurs seems rather more complex, with plenty of cranial crest distribution patterns that could be attributed to: MSS, genetic correlation, immature taxonomy, species recognition, weird taphonomy or (my favourite) aliens with a wicked sense of humour. In this case if we are not able to devise at least one reasonably convincing test for MSS then developing a general understanding of ornamentation in dinosaurs is going to be very difficult.

    Refs –

    Bennett, S. C. 1992. Sexual dimorphism of Pteranodonand other pterosaurs with comments on cranial crests. Journal of Vertebrate Paleontology, 12, 422-434.

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  52. 52. Jerzy New 10:11 am 01/9/2012

    @naishd
    “please explain why the crazy-crested pterosaurs were similar in flight habits to the hornbills and kingfishers you have in mind.”
    I don’t argue these two pterosaurs were perfect analogues of hornbills and kingfishers. I simply point that extreme crests are difficult to reconcile with the traditional interpretation of pterosaurs as either gull-like or vulture-like flyers. I point that there are many birds which are not long-distance flyers, no good walkers and still common and succesful clades – some of which may be models for pterosaurs.

    “you say “[V]ery difficult to reconcile with the vision of pterosaurs laying thin-shelled eggs”. Why? (I’m not saying pterosaurs necessarily did practise biparental care, just curious about your logic).”

    The whole idea of MSS is that male can provide resources to just few females, so females need to advertize to males.

    If chicks need to be fed, OK, male can feed only limited number of chicks. If eggs need to be sat upon and incubated, OK, male can cover only limited number of eggs.

    But thin-shelled eggs plus independent young? What limits a male here from servicing every female? Nothing. Consider that possibly male maintained feeding territory. But female cannot prohibit male from letting other females using the territory whenever she is out of sight. Consider that it was a pterosaur male which maintained and protected nesting mound. But a mound with eggs of 10 females is not more difficult for maintaining and protecting that for 1 female. See mound-building megapodes. There is no resource in which females must compete for male attention.

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  53. 53. Jerzy New 10:31 am 01/9/2012

    @Dave Unwin
    Re: Pteranodon longipes.

    Interesting! Pteranodon is unlike other pterosaurs I talk in the previous post. It seems in fact really adapted to passive flight (using air currents). Aerodynamic properties in passive flight are not scalable, change dramatically with size: small flier simply cannot soar. This puts especially big pressure for juveniles to grow to the adult size as fast as possible. Second, I read (again uncertain how well it was proven) that juvenile Pteranodon really grew to adult size very fast.

    So lifestyle of Pteranodon really makes in a good candidate to evolve posthatching care of young, then co-opt a male into care and females to evolve MSS. A sort of strategy we see in modern albatrosses.

    BTW, I remembered that good old Rhamphorynchus has an ornament on the tail-tip, is known from many individuals and is supposed to grow slowly, implying no post-hatching care. Any chance of dimorphism there?

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  54. 54. Jerzy New 10:45 am 01/9/2012

    BTW,
    The idea of bony crests being replaced by colorful plumage seems not hold – modern birds and mammals use either bony projections, colors, elongated feathers/fur or all together.

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  55. 55. Dave Hone 11:31 am 01/9/2012

    “But thin-shelled eggs plus independent young? What limits a male here from servicing every female? Nothing.”

    Err, what about limited nesting sites? Like those of things like puffins etc. It’s reasonable, even likley that things like Pteranodon and Nyctosaurus were nesting on off-shore islands etc. There may be only room for one nest per male / couple. Limited nesting resources = limited place for eggs = limited number of partners = both genders become very choosy very fast = potential for MSS. Independent young are irrelevant here.

    “BTW, I remembered that good old Rhamphorynchus has an ornament on the tail-tip, is known from many individuals and is supposed to grow slowly, implying no post-hatching care. Any chance of dimorphism there?”

    It’s not ornamental, it’s for steering (or at least inferred to be for a number of good reasons). It’s also not dimorphic.

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  56. 56. Dave Hone 11:39 am 01/9/2012

    ” BTW,
    The idea of bony crests being replaced by colorful plumage seems not hold – modern birds and mammals use either bony projections, colors, elongated feathers/fur or all together.”

    Whao! There’s a lot of conflation of different things in there that we have and haven’t said. Careful now! ;)

    We’re talking about theropods specifically which will be under very different selective pressures (esp predation) to other taxa (as I’ve discussed elsewhere) and could well limit crest size. As such mammals (esp with horns, ie.e. artiodactyls) are a terrible analogy – different selection pressures and I’d hardly call fur analugous to type III feathers. These are not long / large or come in so many colours or can be spreadout or compressed as can wings or fail fans etc.

    Sure yes, oviraptorosaurs and hornbills have both, it’s not complete. But I still would not say it’s unbreasonable that there are some obvious advantages to something like a tail fan or head crest of feathers compared to a fixed bony crest for a theropod. As such, it’s not a massive jump of logic or invalid hypothesis that there could have been a major transition *away* from headcrests and *towards* feather-based displays in the lineage up to birds as a result of the evolution of feathers. Yes we oversimplified the case in the figure and paper, we had to, but you seem to be implying that because the disrtibution of the two is imperfect it has to be wrong. Nope, not at all.

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  57. 57. Henrique Niza 1:59 pm 01/9/2012

    Can we hypothesize using mutual sexual selection that both sexes of ceratopsian chasmosaurines spared with each other and not only males?

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  58. 58. Henrique Niza 2:02 pm 01/9/2012

    P.S.: I meant “sparred with each other”. My apologies.

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  59. 59. naishd 7:19 pm 01/9/2012

    Wow, so many comments. The following was written in response to Jerzy’s discussion of crested pterosaurs (comment 52), but now looks rather redundant given the many new comments – and I do appreciate them all. Anyway…

    1. No matter what you might predict about head crest and behaviour/flight style, it remains the case that some of the pterosaurs with outlandish head crests were (we think, based on strong grounds) albatross-like oceanic soarers. Nyctosaurs, for example, combined gigantic antler-like crests with a rather frigatebird-like morphology (nyctosaurs even lacked the three clawed wing fingers seen in other pterosaurs, so were almost certainly more aerial in habits that other kinds). Extreme crests do seem odd in view of “traditional interpretation of pterosaurs as either gull-like or vulture-like flyers”, but them’s the facts.

    2. You are correct that female showiness and female advertisement of quality often correlate with a style of parenting where males put a lot of effort into reproduction. However, as indicated by the mention of agamid lizards, fruit flies and mosquitoes, MSS doesn’t neatly link to extensive parental care across all groups: “mutual ornamentation may arise because both sexes are forced to compete for mates and mating opportunities in a variety of systems, particularly in polygynous or group-living species” (Tobias et al. 2011). As I said above (comment 45), we don’t know whether pterosaurs practised biparental care or not… but, even if they didn’t, other aspects of their social behaviour could well have been consistent with the presence of MSS.

    Darren

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  60. 60. David Marjanović 7:06 am 01/10/2012

    It’s not ornamental, it’s for steering (or at least inferred to be for a number of good reasons). It’s also not dimorphic.

    Can its shape change during ontogeny (low rudder to diamond to rounded triangle) be explained as necessary to maintain the steering function across different body sizes?

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  61. 61. Dave Hone 7:32 am 01/10/2012

    Not sure, no one has looked at it in great detail as yet. I’m not into rudder theory enough to say, although I’ve been assured by an aeroengineer than all the various shapes seen should function. I suppose it’s far from impossible that it could be dual functional, though I’d argue that if the tail was that critical a signal it would have been retained in the pterodactyloids, or would have gotten much bigger and more elaborate in the basal taxa.

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  62. 62. John Harshman 3:25 pm 01/11/2012

    Darren,

    If there’s a theory of the reason for sexual selection on females that doesn’t involve some form of high male parental investment (not necessarily parental care), I would like to know of it. If males are not in some way a scarce resource, what would make them choosy, or make females compete for them?

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  63. 63. naishd 4:55 am 01/12/2012

    John (comment 62): I didn’t say (in comment 59) that there are cases where MSS “doesn’t involve some form of high parental investment”; rather, that it doesn’t necessarily link with parental care (contra what Jerzy was saying). The mosquitoes, for example, that exhibit MSS don’t practise any parental care, so why the MSS? “Females may benefit from attracting males at a younger age, in more secluded perching sites or from attracting a larger number of courting males which they can then choose between” (South & Arnqvist 2011, cited above).

    Darren

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  64. 64. John Harshman 3:52 pm 01/12/2012

    Ha. That’s puzzling. Why should female ornament matter when attracting males, or attracting a large number of males, unless males are choosy? The standard sperm-dispensing male should attempt to mate with every female he sees.

    Or perhaps these ornaments just make females easier to find? If so, that’s a reason not involving high parental investment at all, and so is interesting. Males are a limited resource only because they’re difficult to locate.

    Similarly, semelparous males ought to be choosy also, thus causing sexual selection in females. Again, the limited resource is the male himself.

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  65. 65. John Harshman 3:55 pm 01/12/2012

    Then again, many semelparous males are so only because they expect to have only one mating opportunity. Males should be choosy only if the number of mating opportunities is high with respect to the number that can be exercised. If, for example, your mate bites your head off and eats you during mating, but there are many potential mates around, it pays to pick that mate carefully.

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  66. 66. ChasCPeterson 10:21 am 01/14/2012

    I apologize–my previous comment was intended more as observation than criticism, but in any case most of the problem turns out to be in my reading.
    There is a common misunderstanding out there that ‘sexual selection’ means ‘mate choice’, and for that reason I think it’s worth applying the label explicitly to stuff like “intraspecific fighting and display”.
    I did not mean to imply that the authors were guilty of the misunderstanding.

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  67. 67. MikeTaylor 8:46 am 01/19/2012

    From the paper (p13): “The apparent absence of cranial ornamentation in sauropodomorphs is interesting in view of the presence, and indeed prevalence, of crests in other dinosaur lineages.”

    Well. The absence of ossified cranial ornamentation. It seems likely to me that many extinct animals, sauropods included, had flamboyant soft-tissue display structures such as wattles, or the crests of cockerels.

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  68. 68. sci-guy 8:51 pm 07/10/2012

    This is a very intersting post and an interesting topic. It has long been understood in the process of sexual selection that males display certain secondary sexual charateristics for the purpose of attracting mates, but this is the first time that I have heard this in dinosaurs.

    It makes sense that just like other animals, notably primates, we would see certain characteristcs that serve no other function than only attarcting mates.

    What would have been intersting as well is to discuss more in depth, how predation may have played a role as certain secondary traits may have been costly. We are unfortunately unable to fully understand the costs and benefits of these traits as we have no way of observing them, but if we look at current species we can hypothesize that there were probably a signiifcant amount of costs associated with such phenotypes.

    Obviously some dinosaurs had weaponry but to what extent the sexes differed in weaponry and to what degree is hard to complete understand but is definetly up for further discussion.

    Very intersting read!

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  69. 69. cgvervaeke 9:25 pm 07/11/2012

    I am recently taking a course in sexual selection and came across your research which I found very similar to topics discussed in my class. If mutual sexual selection was common for ornithodiran evolution, could we predict that intersexual selection was more effective in reproductive success than intrasexual selection?

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