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Dinosaurs and their ‘exaggerated structures’: species recognition aids, or sexual display devices?

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A selection of flamboyant ornithischian dinosaurs. Why were so many dinosaurs so very flamboyant? So that they could tell each other apart, or because - like many living flamboyant animals - their evolution was dominated by sexual selection? Image by Darren Naish.

Mesozoic dinosaurs of several lineages famously possessed horns, frills, bony bosses, crests, frills, blah blah blah – you’ve heard all this a million times before. Pterosaurs were flamboyant creatures too. Why did these animals possess these so-called exaggerated structures? Together with Dave Hone, I’ve just published my latest missive on this issue (Hone & Naish 2013).

As discussed in previous Tet Zoo articles (see links below), I’m one of several researchers who thinks that exaggerated structures evolved primarily under sexual selection pressure: that is, the evolution of horns, frills, crests and so on was driven by the use of such structures in advertising genetic fitness. In wooing mates and intimidating rivals. There are several reasons for favouring this hypothesis: the structures concerned are anatomically similar to those of modern animals that use their structures in sexual selection; the structures exhibit growth rates suggestive of a sexual role; they are frequently costly in terms of growth and maintenance and hence very different from the zero-cost signals associated with other roles, and so on (Knell et al. 2012).

Just some of the elaborate cranial ornamentation present in non-avialan dinosaurs. Images by Dave Hone.

Sexual selection (the set of evolutionary phenomena that are relevant to the enhancing of mating success and fertilisation) is typically imagined to be distinct from natural selection (the set of evolutionary phenomena related to predator avoidance, feeding and foraging, surviving the rigours of climate, and so on). Indeed, the two phenomena frequently operate in contradiction. Palaeontologists have tended to dislike the idea that sexual selection might explain the evolution of exaggerated structures, and have instead proposed that crests, frills, sails and so on evolved within the context of natural selection, most typically as heat-shedding or heat-absorbing structures, or as organs with special aerodynamic or mechanical roles.

An idea that’s been popular among palaeontologists is that exaggerated structures served a special role in species recognition: that is, that they functioned as visual badges allowing members of a given species to recognise conspecifics and differentiate them from heterospecifics. The dinosaur literature basically frames this hypothesis as an alternative to the sexual selection one, at the same time downplaying the sexual selection hypothesis as problematic and without good support.

Do exaggerated structures present in living animals function in 'species recognition' of the sort so often hypothesised for non-avialan dinosaurs? No, the evidence mostly shows that they've evolved - and function - under sexual selection pressure. Veiled chameleon (Chamaeleo calyptratus) image in public domain; Double-wattled cassowary (Casuarius casuarius) by safaris, licensed under Creative Commons Attribution 2.0 Generic license; Anolis (or Norops) polylepis image by Steven G. Johnson, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

One major, crippling problem with the species recognition hypothesis is that crests and other exaggerated structures have yet to be shown to play a role in species recognition in any of the extant animals that have them (Knell & Sampson 2011). Yes, you read that right: feel free to read it again and allocate it to memory. Species recognition does not appear to be an important function for the horns, frills, antlers and so on of chameleons, hornbills, cassowaries, rhinos, deer, bovids, rhino beetles and whatever other extant animals you might consider as possible analogues for ornamented dinosaurs! Instead, the animals use those structures in (drumroll) sexual selection, which is partly (though not entirely) why I and my colleagues prefer the sexual selection hypothesis over others (Hone et al. 2012, Knell et al. 2012, 2013, Hone & Naish 2013). [In montage above, anole by Steven G. Johnson; cassowary by safaris.]

Cover of TREE featuring Knell et al. (2012). Image (featuring male and female Pteranodon with obvious sexual dimorphism) by Mark Witton.

Our latest paper is devoted to a discussion of the species recognition hypothesis and, specifically, why we think it’s problematic and should be discarded. We’ve noted that dinosaur workers have increasingly taken to mentioning species recognition whenever they discuss exaggerated structures (see list of citations in Hone & Naish 2013), so now is a good time to try and set the record straight.

Interested parties will also know of the recent exchange of views that occurred in Trends in Ecology and Ecology between our group and Kevin Padian and Jack Horner (Knell et al. 2012, 2013, Padian & Horner 2013). This debate mostly concerns what we mean by ‘sexual selection’. I’ve already said above what I think it means; Padian & Horner (2013) argue that sexual selection should be applied only to the phenomenon that encourages the evolution of sexually dimorphic traits used in attracting mates or repelling rivals. They lean heavily on the idea that Darwin “invented sexual selection” (Padian & Horner 2013, p. 1): seeing as this is science, not dogma, we disagree with the notion that Darwin’s interpretation is sacred and that it should be adhered to above all else. In any case, Darwin did not (so far as we’ve been able to work out) state anywhere that he regarded sexual dimorphism as key to sexual selection. On the contrary, he even referred to the idea that sexual selection might well exist in cases where dimorphism is absent (Knell et al. 2013, p. 1).

Sexual dimorphism is over-rated. Males and females can BOTH be showy. Exhibit A: Great crested grebes (Podiceps cristatus). Image by Marek Szczepanek, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

And we absolutely reject Padian & Horner’s (2013) argument that sexual dimorphism is essential for the recognition of sexual selection: there’s unambiguous evidence from the living world that sexual selection is at play even when dimorphism is absent (Hone et al. 2012, Knell et al. 2012, 2013). [Adjacent photo by Marek Szczepanek.]

Moving on, which arguments have been put forward in support of the species recognition hypothesis, and how do we respond to them?

‘Directionality’ and ‘randomness’ in phylogeny

One argument is that the exaggerated structures present in dinosaurs seemingly evolved in a “relatively random” pattern, and it’s this random pattern that’s supposedly better indicative of species recognition (Padian & Horner 2011). After all, say Padian & Horner (2011), the point of the exaggerated structures within this context is that they serve to distinguish members of a species from its closest relative(s), and hence any anatomical variation that performed that job was evolutionarily advantageous.

Simplified gamebird phylogeny (based on Bonilla et al. 2010). There are some patterns here as goes the distribution of elaborate display structures, but other structures seemingly appear and disappear at random, with assorted independent losses and gains across phylogeny. Images by Naish (Meleagris), in public domain (Afropavo) or licensed under Creative Commons Attribution-Share Alike 3.0 Unported (Footwarrior: Lophura; Bjørn Christian Tørrissen: Chrysolophus; Doug Janson: Tragopan; Dinesh Kannambadi: Pavo; Dante Alighieri: Polyplectron) and 2.0 (Gary Noon: Phasianus; David Galavan: Perdix; Lip Kee Yap: Gallus) and 2.5 Generic (André Karwath: Coturnix) licenses.

However, our argument (Hone & Naish 2013) is that phylogenies are frequently tremendously ambiguous as goes the ‘directionality’ of exaggerated structures, so much so that you can say whatever you want about randomness. Knell & Sampson (2011) used a similar argument. As an example, there’s little (or no) doubt that the elaborate facial wattles, iridescent neck feathers, long tail feathers and so on of gamebirds have major roles in sexual selection. Yet, when mapped onto phylogenies, these structures seem to appear and disappear at random, with numerous independent losses and gains (e.g., Bonilla et al. 2010). In other words, the claim that randomly arranged exaggerated structures are more in keeping with a species recognition role than a sexual selection one is erroneous.

And, in keeping with what I just said about directionality, things are complicated when we look at Mesozoic dinosaurs anyway, since there are always trends in the evolution of their exaggerated structures that fit with the idea that exaggerated structures become more elaborate (and hence arguably ‘sexier’) over time. We use centrosaurine horned dinosaurs as an example (Hone & Naish 2013). Witness that, within this clade, we see a loss of brow horns and their replacement by a cornified supraorbital pad, a shortening of the nasal horn and its conversion to a gigantic nasal boss, an elaboration of big scales anterior to the nasal boss, and so on (Hieronymus et al. 2009).

In short, there’s no clear support from the ‘directionality’ or diversity of exaggerated structures for the species recognition hypothesis; their diversity and evolution is better consistent with roles in sexual selection.

Friends and relatives: the argument from sympatry

There are numerous cases in the modern world where numerous extremely similar species occur in sympatry: here are the infamous Empidonax tyrannids of North America. How do they tell each other apart without exaggerated structures? Well, they use pigmentation, body size, shape, acoustic cues and so on. Illustrations from the National Geographic Field Guide to the Birds of North America.

A cornerstone assumption of the species recognition hypothesis is that the exaggerated structures of the animals concerned are most prominent in sympatric species (that is, in species that lived alongside one another) (Padian & Horner 2011). Seen the other way round, the argument here is that a diverse array of exaggerated structures in sympatric species indicates the role of such structures in species recognition among those respective animals. We think that several observations make this argument moot: that is, the presence, evolution and elaboration of exaggerated structures fits with the concept of sexual selection, not with species recognition.

Contemporaneous iguanodontians of Early Cretaceous Europe (in this case - from top to bottom - Iguanodon bernissartensis, Dollodon bampingi, Mantellisaurus atherfieldensis: the second may be synonymous with the third). Look, no exaggerated structures! Image by Greg Paul.

Firstly, living animals show that you don’t need exaggerated structures in order to differentiate conspecifics from heterospecifics. Consider that there are numerous extremely similar, sympatric frog, mammal, lizard and bird species that successfully do this without exaggerated structures (they use other cues, like body size, pigmentation, scent, vocalisations and so on). Indeed, among Mesozoic dinosaurs, there are sympatric species that seem to have distinguished one another just fine without the use of exaggerated structures: look at the contemporaneous iguanodontians, for example, that inhabited various Early Cretaceous ecosystems in Eurasia and North America (Hone & Naish 2013). In short, the whole idea that exaggerated structures are needed for species recognition is highly suspect – these elaborate organs are more in keeping with sexual selection.

Secondly, what about those dinosaur taxa bearing exaggerated structures that occur on their own, without close relatives? Examples: the Asian spinosaurid Ichthyovenator, the Chinese stegosaur Wuerhosaurus/Stegosaurus homheni. While the presence of unknown, as-yet-undiscovered related species remains possible, the existence of these singletons would seem to show that species recognition is not the mechanism that’s driving the existence of exaggerated structures in these cases.

The number of contemporaneous stegosaur species present in the Morrison Formation differs substantially between authors, meaning that there are disparate views on how 'species specific' their plates and spines are. Illustration by Darren Naish.

Thirdly, sympatric dinosaurs species are not always obviously distinct in term of the morphology of their exaggerated structures, as they should be if species recognition was the key function of those structures. We use the apparently contemporaneous ceratopsians Protoceratops hellenikorhinus, Bagaceratops and Magnirostris as examples: these animals are not obviously and reliably distinct in frill and nasal boss anatomy “leaving us to wonder how the animals themselves might identify conspecifics if externally visible morphology was their only guide” (Hone & Naish 2013, p. 5). Other examples come from the plates and spines of contemporaneous stegosaurs, the cranial crests of oviraptorosaurs, and the cranial bosses and hornlets of tyrannosaurs.

Numerous flamboyant structures: good for sexual selection, redundant for 'species recognition'. Exemplified here in male Mandarin duck (Aix galericulata). Photo by Darren Naish.

Furthermore, a species recognition role for exaggerated structures indicates that species would differ with respect to the form of a single structure. Instead, however, we see numerous different signals that would be redundant in this context. “In ceratopsians, for example, we see elaboration in nasal horn, brow horn, jugal boss and frill midline and frill edge morphology (in addition to differences in body size, proportions, and integumentary anatomy!)” (Hone & Naish 2013, p. 5). Living animals verify that these multiple signals are better in keeping with the sexual selection hypothesis where, basically, the showier you are, the better (look at the adjacent Mandarin duck Aix galericulata).

According to the species recognition hypothesis, then, these dinosaurs have evolved (frequently) costly and almost wholly redundant structures in order to distinguish one another when they would have been better off evolving ‘zero-cost’ signals for such purposes (Knell & Sampson 2011, Hone & Naish 2013).

Close relatives that seemingly evolved in allopatry – like the Black grouse (Tetrao tetrix) and Caucasian black grouse (T. mlokosiewiczi) shown here (images by John Gould: in public domain) – can’t have evolved their differences as ‘species recognition’ devices because their differences only evolved >after< their ancestral populations became isolated from one another.

Fourthly, let’s consider how exaggerated structures evolved in the first place. According to the species recognition hypothesis, they’re ‘badges’ that sort species x from species y. Ok, but ‘badges’ of this sort would only be needed if speciation was occurring sympatrically (that is, a single population sorted itself into two). Needless to say, if the structures evolved in allopatric species, they’re redundant within the context of the species recognition hypothesis and can’t be used as evidence in its support.

So, we have to think in terms of sympatric speciation when considering the species recognition hypothesis. The only model we can imagine here (Hone & Naish 2013) is that members of the ancestral population evolved incipient versions of the respective exaggerated structures; other members of said population then decided to mate preferentially with those ornamented individuals… eventually, speciation occurred. However, if we’re talking about individuals choosing ornamented individuals over unornamented ones, the ornaments obviously evolved within the context of sexual selection and ‘species recognition’ cannot be considered integral to their origins.

No sexual dimorphism, so no sexual selection. Wait… what?

Another argument used to support the species recognition hypothesis is that an absence of sexual dimorphism in dinosaurs negates the sexual selection hypothesis (Hieronymus et al. 2009). This ‘no sexual dimorphism, thus no sexual selection’ thing keeps on coming up at the moment and it’s utterly erroneous.

No sexual dimorphism, but obvious sexual selection: the case of the Crested auklet (Aethia cristatella). Image by Darren Naish (from Hone et al. 2012).

Firstly, it’s often impossible to be sure that sexual dimorphism truly is absent in fossil animals: the sample sizes we’re working with are frequently just not good enough. Secondly, even in those cases when we can be confident that sexual dimorphism was absent, the possible existence of mutual sexual selection (the phenomenon whereby individuals of both sexes are ornamented) means that sexual selection is still at play.

Like many of the phenomena discussed here, mutual sexual selection is well established and uncontroversial among biologists: it’s fairly widespread in birds and hence our proposal that it might also have been widespread in other dinosaurs (Hone et al. 2012) is not only intriguingly but theoretically reasonable.

Ontogenetic morphing and species recognition: wait a minute… aren’t those concepts incompatible?

If Triceratops really does 'morph' into Torosaurus, then breeding populations of horned dinosaurs encompassed a significant amount of anatomical variation. Is this consistent with the idea that frills and horns evolved as 'species recognition' devices? Image by Nick Longrich.

Jack Horner is one of the primary proponents of the species recognition hypothesis in dinosaurs. As is well known, Horner also advocates the hypothesis that certain dinosaurs (most notably chasmosaurine ceratopsians and pachycephalosaurs) underwent profound anatomical changes during ontogeny. So – to take the most famous example – short-frilled Triceratops underwent a major change in morphology at some stage during adulthood, morphing into long-frilled Torosaurus. Note at this point the evidence (from medullary bone) showing that dinosaurs of many (or most or all) lineages were capable of breeding before reaching full skeletal maturity (Lee & Werning 2008).

If the model of ontogenetic morphing is correct (I agree with others* that it may well not be), we therefore have to imagine dinosaur populations where an anatomically diverse array of individuals are available as mating partners. Within this model, a courting Triceratops thus has short-frilled animals as potential partners as well as long-frilled animals, as well as all manner of intermediates. In other words, it’s faced with several transforming morphs, the more disparate of which are more different from one another than some are from the members of other species.

* Farke (2011), Longrich & Field (2012).

In short, the ontogenetic morphing hypothesis is in direct contradiction with the species recognition hypothesis since the latter requires that members of a species are enough alike that we can obviously identify the anatomical features that allowed them to distinguish conspecifics from heterospecifics. By the way, the notion of late ontogenetic development of a given anatomical structure is not incompatible with a role for such structures in sexual selection (Knell et al. 2012).

Species recognition bad; sexual selection good

Lest we forget, archosaurs aren't the only showy animals. Bovids (like this Black wildebeest (Connochaetes gnou)) can be showy as hell too. Are those display structures for 'species recognition'? (clue: no).

Mesozoic dinosaurs (and pterosaurs, and other fossil animals) were surely capable of distinguishing conspecifics and heterospecifics. The point is that they clearly didn’t ‘need’ to evolve exaggerated structures – horns, frills, bony plates, dorsal sails and so on – in order to do this, and all of the arguments put forward in defence of this idea either don’t support it, or are equivocal and just as likely associated with sexual selection. There’s no obvious support from phylogenetic ‘randomness’ that exaggerated structures evolved within the context of species recognition, a workable model of species recognition that disavows a prominent role for sexual selection has yet to be proposed, claims that subtle or absent sexual dimorphism disproves the existence of sexual selection are false, and the ontogenetic morphing thought to occur in dinosaurs is inconsistent with the species recognition hypothesis. Furthermore, living animals show that exaggerated structures are more to do with sexual selection than species recognition.

I don't think anybody doubts that non-avialan dinosaurs courted, and mated with, conspecifics (and - shock horror - heterospecifics on occasion). The question is: did their mating preferences drive the evolution of their showy, often, elaborate structures? Image by Darren Naish.

As is so often the case with the biology of extinct animals, we know so little that a possible role for species recognition in the evolution, persistence and elaboration of exaggerated structures cannot be ruled out entirely.

However, our primary argument is that there’s “no good evidence that might support this hypothesis and it should not currently be considered viable” (Hone & Naish 2013, p. 7). As I and my co-authors have argued in previous papers (Hone et al. 2012, Knell et al. 2012, 2013), the exaggerated structures of dinosaurs (and pterosaurs) are better explained by a role in sexual selection (and sexual selection should not be used in the peculiar and restrictive definition recommended by Padian & Horner (2013)).

I somehow doubt that we’ll get some members of the community to give up on their idea that the term ‘sexual selection’ means something far more restrictive that the understanding of the term favoured by myself, my colleagues and, I think, the vast majority of biologists who work on this subject. But I do hope that we’ve presented a serious challenge to the species recognition hypothesis. At the very least, dinosaur workers should think very carefully before they claim – as they so often have – that it represents the best explanation for the evolution of exaggerated structures.

For previous Tet Zoo articles on sexual selection and related aspects of Mesozoic archosaur behaviour and biology, see…

Refs – -

Bonilla, A. J., Braun, E. L. & Kimball, R. T. 2010. Comparative molecular evolution and phylogenetic utility of 3’-UTRs and introns in Galliforms [sic]. Molecular Phylogenetics and Evolution 56, 536-542.

Farke, A. A. 2011. Anatomy and taxonomic status of the chasmosaurine ceratopsid Nedoceratops hatcheri from the Upper Cretaceous Lance Formation of Wyoming, U.S.A. PLoS ONE 6, e16196.

Hieronymus, T. L., Witmer, L. M., Tanke, D. H. & Currie, P. J. 2009. The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures. Anatomical Record 292, 1370-1396.

Hone, D. W. E. & Naish, D. 2013. The ‘species recognition hypothesis’ does not explain the presence and evolution of exaggerated structures in non-avialan dinosaurs. Journal of Zoology doi:10.1111/jzo.12035

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

Knell, R., Naish, D., Tomkins, J. L. & Hone, D. W. E. 2012. Sexual selection in prehistoric animals: detection and implications. Trends in Ecology and Evolution 28, 38-47.

- ., Naish, D., Tomkins, J. L. & Hone, D. W. E. 2013. Is sexual selection defined by dimorphism alone? A reply to Padian and Horner. Trends in Ecology and Evolution

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

Lee, A. H. & Werning, S. 2008. Sexual maturity in growing dinosaurs does not fit reptilian growth models. Proceedings of the National Academy of Sciences 105, 582-587.

Longrich, N. R. & Field, D. J. 2012. Torosaurus is not Triceratops: ontogeny in chasmosaurine ceratopsids as a case study in dinosaur taxonomy. PLoS ONE 7, e32623

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

- . & Horner, J. R. 2013. Misconceptions of sexual selection and species recognition: a response to Knell et al. and to Mendelson and Shaw. Trends in Ecology and Evolution 28,

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 He has been blogging at Tetrapod Zoology since 2006. Check out the Tet Zoo podcast at!

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

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  1. 1. JAHeadden 8:54 pm 04/21/2013

    My only two points on this subject are references to the fossil record:

    It is problematic to assume the fossil record is complete enough to make any assumptions on diversity and distribution of taxa within it, such that finding “rare” animals may be problematic due to sampling or geographic biases. Your own work discussing azhdarchids and inland terrestrial stalkers, thus biased against leaving remains, should underscore this. We _probably_ don’t have ANY idea how diverse an ancient ecosystem really is. This is no more relevant than in the Morrison or Dinosaur Park Formations, which, like the Hell Creek, were very diverse from bottom to top, with distinct distributions of taxa from one end to the other. This, coupled with nomenclatural ambiguity (as you mention with stegosaurs) should lead one to immediately sit back and start thinking twice about whether perceived diversity equals actual diversity.

    That said, for most of this topic, I agree with you.

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  2. 2. John Harshman 8:59 pm 04/21/2013

    I suppose the reluctance to attribute some feature to sexual selection is that it’s been the traditional default assumption for structures whose purpose is unknown. But the same would hold true for species recognition signals, so if that’s the choice, there’s no choice.

    I wonder if population variation would help us to distinguish. We would not expect more variance in species recognition features than in any other randomly selected feature. Less, perhaps. On the other hand, any sexually selected feature without variance is pointless. So, a prediction: postulated sexually selected features should show significantly more within-population variance than should randomly chosen features, while species recognition features should not.

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  3. 3. naishd 9:16 pm 04/21/2013

    Jaime: yes, a fair point. However, we can only base conclusions on the data we have. If, say, you only have one dinosaur with exaggerated structures in an assemblage, is it really wise to invoke species recognition? I hope you see my point.

    John: yes, there’s a famous quote from Brian Regal where he says that sexual selection has unsatisfactory explanatory powers since it basically allows you to ‘explain away’ any weirdness without testing it further (we responded to this in Knell et al. 2012 – let me know if you want more details).

    Your comments about variation are probably correct – it is theoretically proposed that species recognition devices are ‘zero cost’ (or close to it) and hence typically unassociated with health and condition, whereas the same is obviously not true for sexually selected characters (indeed, fluctuating asymmetry and condition-dependent stunting are common in the sexual display organs of living animals). What do we see in fossil dinosaurs? Again there’s the caveat about sample size, but we see intrapopulational variation of the sort you’d expect for sexually selected display organs (examples: brow and nasal horns in Triceratops, orbital bosses in Tyrannosaurus, plate form in Stegosaurus).


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  4. 4. greg_t_laden 9:51 pm 04/21/2013

    Ya, I think species recognition is way overrated as a thing. Having said that, some primates really do seem to do it, but they are probably still just showing off.

    A comfortable (to me) hypothesis is that it isn’t species recognition but honest advertising (through handicap) that is working between groups or even between species in resource competition. That might look the same as species recognition in many of the ways you suggest.

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  5. 5. John Harshman 10:00 pm 04/21/2013

    I think a test would be worth doing, but you do need to compare variance in many characters, some proposed to be sexually selected and some not, in order to do a statistical test. Small sample size is of course a potential problem.

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  6. 6. Mythusmage 11:16 pm 04/21/2013

    Why is it only humans that can multitask?

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  7. 7. Heteromeles 11:37 pm 04/21/2013

    You know, I have a lousy sense of smell, and I still have no trouble distinguishing between a cat, a dog, and a human.

    Then I look at those dinosaur skulls most of which have huge nasal cavities, and wonder why people ignore them as functional structures?

    It boggles the mind to think that those dinosaurs never used smell as a species identifier. Granted, the size of olfactory bulbs apparently varied widely, but if tyrannosaurs were using olfaction to find prey, then I’m pretty sure than different dinosaurs smelled different.

    This being the case, why are we arguing that dinosaurs invested in a bunch of incredibly expensive single-purpose visual signs for the sole purpose of identifying their different species? It also appears that birds have largely lost their sense of smell, so bird coloration is clearly not a good analog for dinosaurs in terms of species recognition.

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  8. 8. 11:51 pm 04/21/2013

    If we’re using the Biological Species Concept here, then I’m a little confused as to what, exactly, the difference between sexual selection and species recognition is. If unique character A makes individuals of species X more attractive to other members of X, then surely it also serves to ensure that members of X are only attracted to other members of X (since they’re the only ones that exhibit A).

    I feel like there may be an important distinction, but I’m not quite seeing it. Could you clarify?

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  9. 9. John Harshman 12:36 am 04/22/2013

    Very important distinction: species identifiers do just that, and don’t distinguish among individuals within species; but sexually selected characters are exactly for the purpose of distinguishing among conspecific individuals.

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  10. 10. phalaris 1:35 am 04/22/2013

    Excellent article….many thanks.

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  11. 11. LeeB 1 2:53 am 04/22/2013

    Mutual sexual selection suggests that there are costs to both sexes in raising offspring, and thus reasons for both sexes to attempt to choose (and attract) the best mates.
    Thus in species showing mutual sexual selection might both sexes be provisioning or guarding the young, or guarding territories?


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  12. 12. Tayo Bethel 3:59 am 04/22/2013

    How does mutual sexual selection work in birds? One hears all about how the females show preference for showy males … and hardly anything about male mate choice. The impression one gets is that males will mate with just about any female that comes along.

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  13. 13. naishd 4:08 am 04/22/2013

    Thanks for great comments, everyone.

    Lazy response to questions on mutual sexual selection is to direct you to the lengthy Tet Zoo article on this very subject. MSS might evolve as a side-effect of genetic correlation between the sexes, it might occur because females need to compete for resources as much as (or more than) males do, or it might be there because females are under similar selection pressures to males. In species where both sexes contribute to parenting, males may need to be choosy about partners just as much as females are – in such cases, males are not just indiscriminate sperm-producers who mate with anything.


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  14. 14. Dartian 5:14 am 04/22/2013

    you don’t need exaggerated structures in order to differentiate conspecifics from heterospecifics. Consider that there are numerous extremely similar, sympatric frog, mammal, lizard and bird species that successfully do this without exaggerated structures (they use other cues, like body size, pigmentation, scent, vocalisations and so on)

    Nitpick: some, at least, of those latter cues may be exaggerated structures too – they’re just not anatomical structures. Bird song is a good example; many species have songs that are structurally far more complicated (i.e., exaggerated) than what they would need to be. Of course, the presence of such behavioural, physiological or soft-tissue morphological characters can, alas, only rarely be demonstrated in fossil taxa.

    Another point worth keeping in mind: (Heteromeles already hinted at it, but it’s worth repeating): we humans may generally tend to overemphasize the importance of visual sexual signals. For other species, chemical, acoustic or tactile signals may be of much greater importance when sending and receiving such information.

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  15. 15. jtdwyer 6:32 am 04/22/2013

    I don’t understand the position of anyone arguing against sexual selection, but it seems one has only to observe the role that flamboyant displays play in mate selection processes of reptiles and birds to definitively determine the issue.

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  16. 16. naishd 7:26 am 04/22/2013

    Dartian (comment # 14): you’re correct.. however, in this article (and in the paper it discusses), ‘exaggerated structures’ is used specifically as code for ‘flamboyant anatomical structures’.

    jtdwyer (comment # 15): I wholly agree, which is why I am somewhat mystified by the statements made by some palaeontologists. They seem to want the structures concerned to have any role, so lot as it’s not a sociosexual one.


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  17. 17. John Harshman 9:53 am 04/22/2013

    Mutual sexual selection is possible when both sexes are selling a costly resource and need to be discriminating in the price they receive for it. Sperm, generally speaking, is not a costly resource and so males are not especially concerned about who buys it. But males in many species also offer parental care and thus should be concerned about the quality of the female in whose chicks they invest that care. And thus monogamous pair-bonding often results in assortative mating, with the highest quality male forming a bond with the highest quality female, and so on. But social monogamy isn’t the same as genetic monogamy. That male, in addition to his social mate, may also father many of the offspring of other local females. Females, on the other hand, may need ornaments to attract social mates and thus receive parental care for their chicks, but may still get a little freely dispensed genetic material on the side.

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  18. 18. ChasCPeterson 7:24 pm 04/22/2013

    You make a convincing case, though preaching to the choir in my case (well, one of the baritones).

    Two responses:
    First, the distinction drawn here is, I think, misleading to the point of incorrect:
    “Sexual selection (the set of evolutionary phenomena that are relevant to passing on genes) is typically imagined to be distinct from natural selection (the set of evolutionary phenomena related to predator avoidance, feeding and foraging, surviving the rigours of climate, and so on).”

    This makes it sound as if natural selection is about life and death while sexual selection encompasses everything about reproduction, including fecundity, primary mting apparatus, parental care, etc.
    I was happy to see that the Knell et al. paper uses the more restrictive and, afaik, correct definition of sexual selection: “the process whereby traits are selected because they enhance mating or fertilisation success”. This means phenotypic features that affect mate choice, intrasexual competition for mates, and sperm competition only.

    Otherwise a really interesting read, and the comments too. I can see how mutual intersexual selection could result from situations that already select for pair-bonding, especially if male parental care is necessary.

    One taxon in which species recognition might be a better explanation for nondimorphic bright coloration (if not crests and horns and protuberances: turtles.

    Link to this
  19. 19. Heteromeles 12:18 am 04/23/2013

    @Dartian: so you’re saying that the species-recognition hypothesis doesn’t pass the sniff test?

    Link to this
  20. 20. Dartian 2:54 am 04/23/2013

    Dartian: so you’re saying that the species-recognition hypothesis doesn’t pass the sniff test?

    Who nose – er, knows? ;)

    Link to this
  21. 21. naishd 3:55 am 04/23/2013

    ChasCPeterson (comment # 18): you’re right, my wording there is too woolly, I will correct, thanks.


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  22. 22. Halbred 1:57 pm 04/23/2013

    I’m always tickled when refutations to Horner’s work are published, and I get the same warm, fuzzy feeling here. And these are important distinctions (sexual selection & sexual dimorphism). I’ve also long been suspicious of “species recognition” as an excuse for crests, horns, antlers, etc., so it’s good to know that explanation doesn’t actually hold weight.

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  23. 23. AlexanderBerg 6:13 pm 04/23/2013

    ok – everyone, look at this:

    In birds there are MANY cases of sexual selection producing sexual display devices.

    There! I just proved dinosaurs have sexual display devices. Wasnt that hard.. ;)

    Link to this
  24. 24. Biology in Motion 10:35 pm 04/23/2013

    “Palaeontologists have tended to dislike the idea that sexual selection might explain the evolution of exaggerated structures, and have instead proposed that crests, frills, sails and so on evolved within the context of natural selection, most typically as heat-shedding or heat-absorbing structures, or as organs with special aerodynamic or mechanical roles…”

    Isn’t that the truth! I still have to explain, often against resistance, why pterosaur frills aren’t rudders. Same with the tail vane in the basal forms. Just one example of how, even *after* experimental refutation published in the literature, some workers refuse to accept that an exaggerated structure doesn’t have some special aerodynamic or mechanical function.

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  25. 25. David Marjanović 4:22 pm 04/24/2013

    I suppose the reluctance to attribute some feature to sexual selection is that it’s been the traditional default assumption for structures whose purpose is unknown. But the same would hold true for species recognition signals, so if that’s the choice, there’s no choice.

    Yep. It’s been joked that palaeontologists (or biologists in general) attribute everything they don’t understand to sexual selection just like how archaeologists attribute everything they don’t understand to religion. The important point here is that hypotheses of sexual selection and of species recognition are in fact testable.

    It also appears that birds have largely lost their sense of smell

    Nope. That’s what people used to think till the end of the 20th century. What’s really going on is that birds don’t use their excrements to mark territories – we’ve been selected for finding territorial boundaries stinky (why get into a fight when you don’t need to), they haven’t. Birds crapping their nests full is not evidence that they lack of sense of smell.

    The cases of kiwis and turkey vultures have been known for some time; more recently, it’s been found that albatrosses (IIRC) navigate in part by smell, and similar discoveries continue to surface.

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  26. 26. vdinets 9:54 pm 04/24/2013

    David: I think you are oversimplifying things a bit. It has been found that some birds have very good sense of smell, but it seems to be specialized to particular compounds (like fish oil in case of storm-petrels), and even with all recent discoveries, its use doesn’t seem nearly as extensive as in mammals. Of course, things might change with more research, but note that most mammals can be attracted by invisible bait while most birds can’t.

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  27. 27. Cameron McCormick 10:43 pm 04/24/2013

    Wow, this “anosmatic avians” concept just won’t stay dead! To quote Caro & Balthazart (2010):

    “[T]here is now clear empirical evidence showing that olfaction is perfectly functional in birds and birds use olfactory information in a variety of ethological contexts”

    Examples of recent research include:

    Krause, E. et al. (2012) Olfactory kin recognition in a songbird. Biology Letters 8(3), 327-329. doi: 10.1098/rsbl.2011.1093

    Amo, L. et al. (2011) Smelling out predators is innate in birds. Ardea 99(2), 177–184. doi:

    Coffin, H. et al. (2011) Odor-Based Recognition of Familiar and Related Conspecifics: A First Test Conducted on Captive Humboldt Penguins (Spheniscus humboldti). PLoS One 6(9): e25002.

    Zelenitsky, D. (2011) Evolution of olfaction in non-avian theropod dinosaurs and birds. Proceedings of the Royal Society B 278, 3625–3634. doi:10.1098/rspb.2011.0238

    Caro, S. & Balthazart, J. (2010) Pheromones in birds: myth or reality? J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 196(10), 751–766. doi: 10.1007/s00359-010-0534-4.

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  28. 28. kilianh 8:14 am 04/25/2013

    @Cameron McC (#27): The fact that it is “perfectly functional” does not mean it is used as extensively, or as broadly, as with mammals. Given that, even after 65My of evolution, most birds are diurnal and mammals nocturnal (greatly overgeneralizing here, but afaik the pattern is clear), mammals smelling better than birds, and birds having better eyesight than mammals, and consequently birds relying more on eyesight is not all that strange (which might also explain the more elaborate display structures of birds).

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  29. 29. kilianh 8:32 am 04/25/2013

    Has anyone ever tried to explain exactly by what known evolutionary mechanism the evolution of exaggerated structures for species recognition can be the result of natural selection?

    The only thing I can come up with is a scenario that has two separate populations of different species that are so identical that they would frequently inter-mate but produce sterile or otherwise unfit offspring, join due some geographical event. However, this is very far fetched and would not happen frequently enough to explain the diversity we are seeing. Also, more subtle clues than the actual elaborate structures would be more than enough.

    Speciation may occur when these structures evolve in part of a population, but sexual selection can be the only pressure then, as there still is a single species, and there’s nothing to recognize yet. It completely baffles me that someone can think that speciation can occur because structures evolved that evolved because of species recognition. That seems circular reasoning…

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  30. 30. Heteromeles 11:14 am 04/25/2013

    My example of an anosmotic bird is personal. Many years ago, I had a pet pigeon (feral bird, got him as a semi-fledged chick with a broken wing, kept him as a house pet). I also had one of those halogen torchiere floor lamps. Said pigeon liked to warm his butt up on the lamp on cold nights. One halloween night in his first year, he charred his tail feathers off on the halogen bulb. The smell was so bad that, after I got him away from the light and clipped the charred ends of his feathers off, I had to leave my apartment for an hour with all the windows open to air it out. Mr. Pigeon? He was falling asleep as his tail charred, due to his nice, warm butt in a cold room. Oh, and I had to replace the lamp, because every time I turned it on after that, it smelled like charring feathers. The burned keratin had coated the bulb.

    My opinion is that if a pigeon can’t smell his own feathers charring, he has no sense of smell. Obviously other birds do have some sense, but it’s pretty silly to conclude that, because some birds can smell, therefore all birds have a good sense of smell. the evidence doesn’t support this notion either.

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  31. 31. David Marjanović 1:25 pm 04/25/2013

    The fact that it is “perfectly functional” does not mean it is used as extensively, or as broadly, as with mammals.

    But that wasn’t the claim. The claim was that it “appears that birds have largely lost their sense of smell”.

    My opinion is that if a pigeon can’t smell his own feathers charring, he has no sense of smell.

    You don’t know if he couldn’t smell it. All you know is that he didn’t find it stinky. Even within humans you can find a wide range of reactions to burnt smells.

    Think of it: fire is generally pretty harmless to a flying bird till it’s close enough to feel the heat. Fleeing from the stench doesn’t provide much of a selective advantage. For a climbing mammal that’s far from true!

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  32. 32. Heteromeles 1:43 pm 04/25/2013

    Um David, would you investigate a new smell coming from behind you? The case here isn’t that he noticed and didn’t care. He didn’t even notice. He certainly saw the damage to his tail as I cut it off, and that disturbed him. In any case, the argument that a bird has an excellent sense of smell, but couldn’t smell anything when his feathers are smoking? Preposterous. It’s not a subtle smell. I’d suggest burning a feather if you don’t believe me.

    In fact, this is an experiment you can easily do with a pet bird and a burning feather that doesn’t belong to the bird. Perhaps you can use a cat or a rat as a control, if you think that humans over-react to that particular smell.

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  33. 33. Cameron McCormick 2:28 pm 04/25/2013

    Pigeon olfactory capabilities are well established.

    Olfactory lateralization in homing pigeons: a GPS study on birds released with unilateral olfactory inputs

    Pheromones in birds: myth or reality?

    Link to this
  34. 34. Dartian 3:12 am 04/26/2013

    it’s pretty silly to conclude that, because some birds can smell, therefore all birds have a good sense of smell

    It is, but then again, nobody actually claimed that here.

    the evidence doesn’t support this notion either

    Not so fast. All birds (or at least all thus far investigated species) possess an olfactory bulb (Bang, 1971). In their nasal cavities, birds also have olfactory epithelia where olfactory receptor cells are situated. In other words, both in terms of gross morphology and neuroanatomy, birds have all the necessary structures required for a decent olfactory capacity. If natural selection has maintained those structures across Aves, we must presume that there is some good reason for that.

    Bang, B.G. 1971. Functional anatomy of the olfactory system in 23 orders of birds. Acta Anatomica 79 (Supplementum 58), 1-76.

    Link to this
  35. 35. Mark Robinson 3:43 am 04/26/2013

    Anecdotal but, I have kept pigeons and can assure everyone that all of mine had a decent sense of smell.

    They didn’t like the smell of my cat on my hands after I had recently stroked her. If I washed my hands first, they were fine. They didn’t seem to care if I had stroked the dog.

    I even tested this once by stroking the dog with one hand and the cat with the other. The pigeons exhibited no noticeable change in behaviour when they were handled or fed with my dog-hand, but were jittery once my cat-hand was brought close enough for them to catch a whiff.

    So, whilst I won’t extrapolate this small personal experience to allow me to make assumptions about all birds, I think it’s reasonable to say that pigeons are able to smell quite well.

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  36. 36. David Marjanović 9:40 am 04/26/2013

    Um David, would you investigate a new smell coming from behind you?

    Depends on a lot of things, actually. If I thought it was a nice new room perfume, I might not investigate. If I didn’t notice it was coming from behind and mistakenly thought it was coming from something I could already see, I definitely wouldn’t investigate further. And so on.

    The case here isn’t that he noticed and didn’t care. He didn’t even notice.

    He didn’t notice what caused the smell. You don’t know if he didn’t notice the smell.

    In any case, the argument that a bird has an excellent sense of smell, but couldn’t smell anything when his feathers are smoking? Preposterous.

    Excuse me? Do I have to quote your own words at you again? Here goes: “It also appears that birds have largely lost their sense of smell.” You can’t get to that conclusion from your example. I never said your pigeon had an “excellent” sense of smell, because I can’t get there from your example either; I said that it’s not true that “birds have largely lost their sense of smell”. That’s all.

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  37. 37. Heteromeles 10:45 am 04/26/2013

    Thanks Mark. This gets even better. Now we’ve got two sets of different birds, one which never gave any evidence of a sense of smell (the burned feathers was the most extreme example), one set that does. Great lesson for those coding data sets, as well as for those who swear that the lack of a sense of smell is a dead myth or a live reality. Oddly enough, there’s probably variation within species, even well-known species like rock doves.

    Link to this
  38. 38. Yodelling Cyclist 12:52 pm 04/26/2013

    With respect to the singed pigeon: isn’t keratin largely made up of cysteine units? My point is that sulfur compounds (particularly the odd thiols I would expect from a poorly controlled oxidation of cysteine in a variety of chemical states/positions in a protein) usually reek to high heaven (at least to mammal noses), but it’s notable that most chemists who work with them long term get to the stage where they don’t notice. Particularly if the build up in the lab is slow. I have no idea why that is biologically – but it is true that nauseating, vomit inducing stenches can be entirely overlooked if you’ve been in the room all the time while the concentration builds up gradually.

    What I mean is: the pigeon may have just overlooked the smell of sulfur compounds as his feathers burned slowly.

    Link to this
  39. 39. llewelly 8:28 pm 04/26/2013

    An alternative hypothesis is that Heteromeles’ bratty pigeon deliberately stank up the room in order to get back at Heteromeles for some real or imagined slight.

    Link to this
  40. 40. Yodelling Cyclist 10:30 pm 04/26/2013

    Sod my suggestion, I prefer llewelly’s.

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  41. 41. David Marjanović 8:01 am 04/28/2013

    My point is that sulfur compounds (particularly the odd thiols I would expect from a poorly controlled oxidation of cysteine in a variety of chemical states/positions in a protein) usually reek to high heaven (at least to mammal noses)

    Crap is full of thiols. That explains our reaction to thiols, I guess.

    Link to this

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