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Terrifying sex organs of male turtles

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


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A Testudo tortoise and its large erect penis.

ResearchBlogging.org

Of the many unlikeable and inaccurate stereotypes maintained about animals in popular consciousness, among the most frustrating is what I term “old man turtle”. This is the idea that turtles (by which I mean, all members of Testudines) are like decrepit, weak, bony little old men housed inside a box. It’s not fair, and it’s not at all accurate. Here we look at just one aspect of turtle anatomy. In keeping with the stupid “old man turtle” idea, popular culture would have it that turtles are weak, flaccid, crappy organisms with dull social lives, stunted and barely functional internal organs and undersized sex organs. Well, wait a goddam minute…

Warning: the following article may be considered unsuitable for viewing by minors.

Believe it or don’t, turtles are horrifically well endowed, and if the thought of learning more about the genitals of these oh-so-surprising reptiles doesn’t appeal to you, look away now. Last warning. Ok, here we go.

Vertebrate penises in cross-section, from Kelly (2002). VS = vascular space; TM = tensile membrane.

Hydraulic intromittent male sexual organs – a variety of popular, alternative names are available – are not unique to mammals among tetrapods. They’re also present in squamates, archosaurs and turtles. This phylogenetic distribution has led some authors to conclude that these organs were present in amniote common ancestors. However, in their details, the organs of these groups are all quite different and actually formed from non-homologous tissues. As shown by Kelly (2002), male intromittent organs therefore arose independently among tetrapods on more than one occasion. The turtle penis, for example, contains only one vascular erectile body and develops on the ventral surface of the cloaca, whereas the mammal penis contains two erectile bodies and is derived from non-cloacal tissue. In the diagram above – from Kelly (2002) – the penises of turtles, birds, mammals and snakes are compared in transverse section. Note how different the organs are in their cross-sectional structure.

Penis or phallus? Ahh, choice

Another view of a Testudo tortoise's penis. Image credited to (c) www.konnamaa.com.

An intromittent organ of this sort is typically termed a ‘penis’. Some researchers suggest that this term should be restricted to mammals and that the convergently similar organs of turtles and archosaurs should be termed phalluses instead (Isles 2009). However, others argue that there’s nothing about the term ‘penis’ that means it has to be restricted in this way, and indeed there’s nothing particularly special about the mammal penis when we compare it with the intromittent organs of other tetrapods. Accordingly, some biologists who publish on intromittent organs consistently term all of these organs penises (e.g., Kelly 2002, 2004, McCracken 2000). Biologists certainly haven’t had a problem in using the term ‘penis’ for the turtle organ in the past (e.g., Zug 1966).

How to build a turtle penis

The turtle penis is, like that of a mammal, a hydraulic cylinder that becomes engorged by fluid and is relatively resistant to bending when erect. Its single erectile body is divided into a collagenous corpus fibrosum and a highly vascularized, expandable corpus spongiosum. As a turtle’s penis inflates, its length may increase by nearly 50%, its width by 75%, and its depth by 10%. Even an uninflated penis – tucked away inside the cloaca – is large. More on the issue of size later on.

More tortoise penis. Spot Hello Kitty.

A pair of long retractor muscles extend for most of the length of the organ’s dorsal surface, and attach within the body cavity to the lumbar vertebrae. When at rest, the penis is doubled up on itself within the cloaca, and it’s the contraction of the retractor muscles that causes it to un-double and protrude (Gadow 1887). During erection, the penis first emerges pointing posteriorly; “as the size and tension increases the penis bends ventrally and then slightly anteriorly” (Zug 1966, p. 4). Bishop & Kendall (1929) found that turtle penis retractor muscles were “physiologically rugged” and of “extreme endurance”.

Collagen fibres reinforce the penis wall and are arranged either along, or perpendicular to, the organ’s long axis, and in this respect the turtle penis is superficially similar to a mammalian one. However, while the mammal penis only has one layer of long-axis fibres, and one layer of perpendicular fibres, the walls of the turtle penis have multiple layers of these fibres. This array of stiffening collagenous fibres is still, however, highly similar in turtles and mammals: as noted by Diane Kelly in the title to her 2004 paper “Turtle and mammal penis designs are anatomically convergent” (Kelly 2004). The strong similarity observed in the erectile organs of these phylogenetically disparate groups suggests that there are few functional solutions permitting the evolution of cylindrical, inflatable intromittent organs (Kelly 2002, 2004). Kelly is well known for her previous work, widely reported in the media, on penis anatomy in armadillos (Kelly 1997) collected as roadkills near Tallahassee, Florida. Her publications can be obtained, free, from her homepage here.

Schematic representations of turtle penis anatomy, from Zug (1966).

In terms of overall macrostructure, the turtle penis consists of a shaft and a distinct head, or glans, that’s typically dark grey, purple or blackish.

A long seminal groove, surrounded on both sides by raised ridges (termed seminal ridges), extends from the urethral opening down at the base of the penis to the glans. Obviously, we’re talking here of an exposed groove, not an enclosed internal tube like that present in mammals. Mammals are actually unusual in possessing an enclosed tube in the penis: seminal grooves are the norm when we look at the organs of lizards and snakes, crocodilians and birds.

The seminal ridges in a turtle are largest right next to the glans; near the glans, they’re surrounded on both sides by fissures, or sinuses. Anterior and posterior pairs of sinuses are also present on the upper surface of the glans. These structures, associated with mobile skin folds, give the glans a decidedly alien-like, unfamiliar look to we primates. Turtles seem to be able to control the movements of the ridges around the seminal groove as well as the openings and folds on the head of the glans. The structures on the upper surface of the  glans can in fact open and close, in ‘flower-like’ fashion, in a sort of pulsing or throbbing motion. There are some especially endearing videos showing this on youtube (the most popular one shows a Red-footed tortoise Chelonoidis carbonaria forming a strong relationship with a rubber ball). However you respond to these images, don’t feel ashamed.

Glans anatomy in a variety of snapping turtles, river turtles, tortoises and other cryptodires, from Zug (1966).

The precise configuration of sinuses and associated folds, and thus the overall form of the glans, varies from group to group (Zug 1966). Some of the configurations involved look terrifying; others look really terrifying. The penis as a whole is seemingly simplest in sea turtles*. Here, the glans is pointed, with the seminal groove terminating in a single, deep fold. In mud turtles (Kinosternidae), big-headed turtles (Platysternon), land tortoises (Testudinidae), and batagurid and emydid river turtles, the glans is broad and fat. In many species, there’s a pointed medial process at the tip of the glans. In land tortoises and the New Guinea pig-nosed turtle (Carettochelys insculpta), the seminal groove is bifurcated at its distal end; in Carettochelys, the tip of the glans has a tri-lobed appearance where each branch of the seminal groove extends distolaterally into its own lateral lobe, separated on the midline by a distomedial lobe (Zug 1966). Carettochelys is odd in lacking sinuses on its penis.

* Some experts prefer to write the name ‘seaturtle’. I don’t think that this suggestion has caught on yet, so will stick with ‘sea turtle’ here (and equivalent terms for other turtle groups).

Glans of Florida softshell (Apalone ferox). It has five lobes and a seminal grooves that branches into four separate channels. From Zug (1966).

Softshell turtles (Trionychidae) go one (or two) better, since their glans is five-lobed. Again, the seminal groove is bifurcated, with each branch leading distolaterally to the tip of a pointed proximolateral structure.  But, before reaching the tip of that proximolateral structure, the groove branches again, with this more distal branch of the groove extending to the tip of a pointed distolateral structure (Zug 1966). Softshell turtles thus discharge semen from four distinct branches of the seminal groove. This might leave you wondering what the insides of a female softshell’s cloaca are like. That’s an issue I should discuss some other time.

Why do we need phylogenies? Why? To give us an evolutionary backbone to hang our hypotheses on, stupid

Incidentally, the anatomically ‘simple’ penis present in sea turtles has sometimes been regarded as  peculiar given that phylogenies typically find this group to be nested fairly deep within Cryptodira (the so-called ‘hidden-necked turtle’ clade). This topology means that sea turtles are surrounded in the phylogeny by softshells, snapping turtles, mud turtles and tortoises and river turtles (e.g., Gaffney & Melyan 1988, Shaffer et al. 1997, Hirayama et al. 2000), all of which have complex penises.

The giant Cretaceous sea turtle Archelon reconstructed with a large penis. Image by D. Naish.

So, is it that the sea turtle penis has become secondarily ‘simplified’ – presumably as a consequence of adaptation to pelagic life – or is it that the different, complex penises present in the other lineages evolved their complexity independently? To be honest, this issue hasn’t been examined in detail in any phylogenetic analysis (to my knowledge). However, Joyce (2007) has more recently found sea turtles to be the sister-group to all remaining cryptodires. If this is correct, it might mean that the simplicity of the sea turtle penis is a primitive feature… but what about pleurodires (the so-called ‘side-necked turtles’)?

Pleurodires – the closest living relatives of cryptodires – aren’t as well studied as cryptodires, and less information is available on their genitalia. What little data I’ve seen (e.g., Cabral et al. 2011) suggests that the penises of some taxa at least are simple (that is, with a slender, pointed glans and little in the way of crazy folds and lobes) and superficially similar to those of sea turtles. My impression at the moment is that pleurodires and sea turtles share a ‘simple’ penis as a symplesiomorphy (= shared primitive character), but this could be very wrong since I’ve seen little information on the pleurodire penis.

How big? BIG

As interesting as it is from the point of view of embryology, phylogeny, microanatomy and detailed anatomy, one thing particularly eye-opening (no pun intended) about the turtle penis is its SIZE. It really is large and formidable in some species. It’s perfectly normal for some tortoise species to have a penis that is half the length, or more, of the plastron. I would guess that in a tortoise with a total length of 20 cm, the penis might be 8 cm long.

Giant tortoises mating. These animals are identified on wikipedia as Galapagos tortoises, but - following help from Jeannot Tihoti Maha'a - I think they're Aldabran giants. Look carefully! Photo by Minglex, licensed under Creative Commons Attribution 3.0 Unported license.

So, small turtles can have proportionally huge organs. What about big turtles? Unfortunately, little data is available. A few days ago, Roger Close asked me on facebook if we know anything about the size of the male organ in Galápagos giant tortoises (Chelonoidis nigra and kin). While mating behaviour in Galápagos tortoises has been filmed many times, I have yet to see any good images of genital anatomy in these animals. Petterer & Neuville (1914) described penis morphology in Aldabran giant tortoises Aldabrachelys gigantea*, but didn’t provide much information. If you have useful data, please say so!

* If you follow these things, I would say that this name has rightfully won out over Dipsochelys dussumieri. Does anyone know if the ICZN has published a ruling yet?

A Leatherback turtle's penis is extracted from its cloaca during dissection on Inside Nature's Giants. Image (c) Windfall Films/Channel 4.

Sea turtles are another group of turtles famous for reaching large size. Surely they have large penises. Yup. In a Green turtle Chelonia mydas (maximum length c. 1.5 m, carapace length c. 80-110 cm), the penis is typically more than 30 cm long (Hamann et al. 2003). Hold your hands 30 cm apart and think about that enormous penis for just a moment. What about the Leathery turtle Dermochelys coriacea? This amazing giant can exceed 2.2 m in total length and have a carapace length of 1.7 m. The original version of the article you’re reading now was published back in 2007, and since then a Leathery turtle Dermochelys coriacea dissection has been featured on TV as part of the fantastic series Inside Nature’s Giants. Unfortunately, I missed it when it was on and haven’t been able to see it yet. Joy Reidenberg told me at the time that the male individual they examined was, indeed, well endowed. As you can see from the screen-shots shown here, she wasn’t kidding. [Thanks loads to Markus Bühler and Emilio Río Rodríguez for help in getting the images at short notice.]

Leatherback turtle penis, revealed during dissection on Inside Nature's Giants. Image (c) Windfall Films/Channel 4.

You have an enormous penis – so, what do you do with it?

While it might seem like a bloody stupid question, you have to wonder exactly what it is that turtles do with these sometimes enormous organs. The evolution of the shell probably means that male turtles were forced to evolve innovative penises in order to make genital contact with their partners. In sea turtles, males have proportionally enlarged, prehensile tails, and the tails of other kinds of turtle are also usually longer and bulkier in males than they are in females. The cloaca isn’t situated at the base of the tail, but some distance along its length, so it seems that part of the distance that the penis needs to reach in order to inseminate the female is covered by tail-reach, not by penis-reach alone. Incidentally, some fossil Cretaceous sea turtles have really long tails – way longer than those of any modern sea turtles. This may or may not mean something for penis anatomy, but I don’t think we’ll ever know.

As is the case in other tetrapods that possess proportionally large sexual organs (including certain ducks, cetaceans and, yes, some primates), observational data suggests that male turtles might employ their organs in display or aggression. Honda (2001) had this to say about captive specimens of the Common box turtle Terrapene carolina

“Sometimes males will distend their organ neither while mating, nor while in the presence of females. Usually while bathing or drinking, the turtle will submerge the front half of his body, rise up on his back legs, and drop his organ through the cloaca. It is a sight to behold, and one that can startle both novice and experienced herpetoculturalists alike. The organ itself is large in proportion to the turtle, and dark purple in color. After several seconds, the turtle will retract the organ back through the cloaca. It may repeat this process once or twice.”

Snapping turtle (Chelydra serpentina) with penis out. A response to being handled.

I also note the very interesting paper by de Solla et al. (2001): “Penis displays of common snapping turtles (Chelydra serpentina) in response to handling: defensive or displacement behaviour?”. [Adjacent photo credited to /r/Pics]. Leatherback turtles are also known to evert the penis as a response to handling (James 2004), and this behaviour has also been reported in pleurodires (Hydromedusa) and other turtles.

However, as tempting as it might be to imagine that some turtles are perhaps in the habit of intimidating enemies or competitors with their erect, 20-cm long, black, spike-tipped penises, it seems more likely that this penis eversion most often occurs as a displacement behaviour, practised when the animal’s plastron is touched. Then again, given what we now know about play behaviour in turtles and other reptiles, it should be considered plausible that turtles expose their impressive genitals for fun, or when bored.

And that is just about everything I know about turtle penises. Well, there’s the TMNT porn, slash fiction and so on that I’ve discovered online, but let’s not mention that. To those of you who recall reading this article the first time round (as I said above, it first appeared at Tet Zoo ver 2 back in 2007), I hope you enjoyed revisiting it in updated, augmented form. To those of you for whom this information is new… I trust that you’ll never look at a turtle in the same way again.

For previous Tet Zoo articles on turtles, see…

Refs –

Bishop, G. H. & Kendall, A. I. 1929. Action of formalin and histamine on tension and potential curves of a striated muscle, the retractor penis of the turtle. American Journal of Physiology 88, 77-86.

Cabral, S. R. P., de Souza Santos, L. R. Franco-Belussi, L., Zieri, R., Zago, C. E. S. & de Oliveira, C. 2011. Anatomy of the male reproductive system of Phrynops geoffroanus (Testudines: Chelidae). Acta Scientiarium: Biological Sciences 33, 487-492.

de Solla, S. R., Portelli, M., Spiro, H. & Brooks, R. J. 2001. Penis displays of common snapping turtles (Chelydra serpentina) in response to handling: defensive or displacement behaviour? Chelonian Conservation and Biology 4, 187-189.

Gadow, H. 1887. Remarks on the cloaca and on the copulatory organs of the Amniota. Philosophical Transactions of the Royal Society of London B 178, 5-37.

Gaffney, E. S. & Meylan, P. A. 1988. A phylogeny of turtles. In Benton, M. J. (ed) The Phylogeny and Classification of the Tetrapods, Volume 1: Amphibians, Reptiles, Birds. Clarendon Press (Oxford), pp. 157-219.

Hamann, M., Limpus, C. J. & Owens, D. W. 2003. Reproductive cycles of males and females. In Lutz, P. L., Musick, J. A. & Wyneken, J. (eds) The Biology of Sea Turtles, Vol. II. CRC Press, Boca Raton (Florida), pp. 135-161.

Hirayama, R., Brinkman, D. B. & I. G. Danilov. 2000. Distribution and biogeography of non-marine Cretaceous turtles. Russian Journal of Herpetology 7, 181-198.

Honda, M. 2001. Chelonian notes. Art Journal 60 (2), 96-100.

Isles, T. E. 2009. The socio-sexual behaviour of extant archosaurs: implications for understanding dinosaur behaviour. Historical Biology 21, 139-214.

James, M. C. 2004. Dermochelys coriacea (Leatherback sea turtle). Penis display. Herpetological Review 35, 264-265.

Joyce, W. G. 2007. Phylogenetic relationships of Mesozoic turtles. Bulletin of the Peabody Museum of Natural History 48, 3-102

Kelly, D. A. 1997. Axial orthogonal fiber reinforcement in the penis of the nine banded armadillo (Dasypus novemcinctus). Journal of Morphology 233, 249-255

Kelly, D. (2002). The Functional Morphology of Penile Erection: Tissue Designs for Increasing and Maintaining Stiffness Integrative and Comparative Biology, 42 (2), 216-221 DOI: 10.1093/icb/42.2.216

- . 2004. Turtle and mammal penis designs are anatomically convergent. Proceedings of the Royal Society of London B 271 (Suppl 5), S293-S295.

McCracken, K. G. 2000. The 20-cm spiny penis of the Argentine lake duck (Oxyura vittata). The Auk 820-825.

Petterer, E. & Neuville, H. 1914. Du penis et du clitoris des crocodiles et des tortues. Rendu Hebdomadaire des Seances et Memoires de la Societe de Biologie, Paris 76, 101-103.

Shaffer, H. B., Meylan, P. & McKnight, M. L. 1997. Tests of turtle phylogeny: Molecular, morphological, and paleontological approaches. Systematic Biology 46, 235-268.

Zug, G. R. 1966. The penial morphology and the relationships of cryptodiran turtles. Occasional Papers of the Museum of Zoology, University of Michigan 647, 1-24.

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. Heteromeles 10:20 pm 06/8/2012

    I was about to ask whether turtles can breathe through their phalluses, as some can through their cloacal bursae. Instead, since some aquatic turtles seem to have simpler phalluses, can I suggest it’s so that their cloacas are clear to get oxygenated water into their bursae? Or is that phallaceous thinking on my part?

    Link to this
  2. 2. vdinets 11:25 pm 06/8/2012

    The ball video is really impressive. I wonder how such a huge structure can possibly fit inside the female. Perhaps the terminal part doesn’t fully extend when it’s inside?

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  3. 3. BrianL 11:54 am 06/9/2012

    One wonders what size phalli *Meiolania* or * Colossochelys* might have sported…

    How likely is that our humongous friends the sauropods also sported both absolutely and proportionally huge phalli? Certainly mating must have been a tricky thing for creatures this size. Similarly, could huge phalli be the solution to the mechanics of stegosaur mating?

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  4. 4. Heteromeles 1:28 pm 06/9/2012

    @Brian: Jinx! Back on 2.0, I made a similar comment about Stegosaurus. I forgot the reason it was shot down, but it was. Sigh. There’s something to be said for the evolution of a large and manueverable phallus, as opposed to vent-to-vent copulation, for many dinosaurs, including sauropods and anklyosaurs. Unless we find the right mummy, we shall never know…

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  5. 5. naishd 1:39 pm 06/9/2012

    Thanks for interesting comments.. I’m hoping for many more (smiley). Comment 1: so far as I know, there’s no indication that the penis is involved in respiration of any sort. For naive audience, we should add here that (as you note) you’re only saying this because you’re familiar with the amazing fact that some turtles are able to use the cloacal interior as a respiratory surface.

    However, I can’t refer to this area without mentioning the bizarre idea from the world of qi (that is, the Chinese art of chi) that men can practise a form of ‘breathing’ where qi is drawn in through the penis and used to activate energy in the sacrum. It’s known as turtle breathing. Here’s a website.

    Darren

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  6. 6. Panimerus 3:27 pm 06/9/2012

    How is the mating systems of the sea turtles with simple penii? In insects the male genitalia are typically much less complex and taxonomically less useful in cases where there is less competition between males for females (e.g. inbreeding bark beetles).

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  7. 7. Panimerus 3:28 pm 06/9/2012

    “Penii” should of course be “penises” as the organ, alas, is not called a penius.

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  8. 8. Suttkus 5:12 pm 06/9/2012

    The turtle leaves twixt plated decks
    That practically conceal its sex
    I think it clever of the turtle
    In such a fix to be so fertile.
    – Ogden Nash

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  9. 9. naishd 5:55 pm 06/9/2012

    One of my friends (Matt Bille) quoted the Ogden Nash poem on facebook earlier today, and here’s what I said in response…

    “You see the stereotypes we’re up against – that Odgen Nash poem is nice, but Nash clearly never spent >any< time with turtles, nor bothered to learn anything about them. I wouldn't say that animals with penises half (or more) of body length, and with vigorous and aggressive sex drives, are at all doing a good job of concealing gender!!"

    I wasn't being entirely serious, but I hope you see my point.

    Darren

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  10. 10. SiaraDelyn 6:19 pm 06/9/2012

    The plural of penis should be penae, shouldn’t it?

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  11. 11. StupendousMan 6:56 pm 06/9/2012

    “Penis” is Latin, third declension. Plural “penes”.

    At last, after thirty years, my high school education is paying off!

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  12. 12. Heteromeles 7:52 pm 06/9/2012

    In Mandarin Chinese, “turtle egg” means “bastard,” because turtles don’t know their fathers and turtles are promiscuous. Perhaps the Chinese pay more attention to turtles than most westerners do?

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  13. 13. Jurassosaurus 7:54 pm 06/9/2012

    “Penis” is Latin, third declension. Plural “penes”.

    At last, after thirty years, my high school education is paying off!

    Yep. It’s rather annoying that the misspelling “penises” is so pervasive now that it is officially considered a proper plural.

    At least the herp guys got it right (i.e. hemipenes). Though as far as I know, that is the only time I’ve ever seen it used properly.

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  14. 14. rickilewis 10:48 pm 06/9/2012

    Thank you for solving the mystery of the gender of my beloved tortoise, Speedy the second. As I’d suspected, she is indeed a she.

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  15. 15. Metridia 11:36 pm 06/9/2012

    Are turtles procolophonids or some other kind of anapsid? I feel like we need a TetZoo exposition of this issue. I know the molecular studies are definitive in showing them nested within diapsida, but seeing as we don’t otherwise have molecular sampling of anapsids, that is not ideal. Anyway, TetZoo has taken up crazier debates in its time, like the BAD crowd and long-necked seals.
    I wonder if the anapsid-like skull is the byproduct of some superossification development program associated with the development of the shell. What does developmental biology say about the development of the turtle skull?

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  16. 16. jtdwyer 4:36 am 06/10/2012

    Just looking at the pictures, it seems clear that mating between these large shelled creatures could only be accomplished from long distances, requiring the lengthy male genitalia…

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  17. 17. tai haku 4:55 am 06/10/2012

    The photo of the mating aldabrans hints at another terrifying aspect of male turtles sex lives – the vocalisation. I took the video below of San Diego’s burmese brown tortoises mating and the noise was unbelievable.
    http://tai-haku.blogspot.com/2008/11/sweet-tortoise-lurvin.html

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  18. 18. David Marjanović 7:16 am 06/10/2012

    the mammal penis contains two erectile bodies

    How widespread are three, then? There’s a ventrally positioned one around the human urethra.

    In Mandarin Chinese, “turtle egg” means “bastard,” because turtles don’t know their fathers and turtles are promiscuous.

    Especially because they can’t see who’s humping them from behind.

    Yep. It’s rather annoying that the misspelling “penises” is so pervasive now that it is officially considered a proper plural.

    Well, that’s simply English as opposed to Latin. What annoys me is the many, many people who don’t know that -ii isn’t an ending at all.

    Are turtles procolophonids or some other kind of anapsid?

    CELEBRITY DEATHMATCH!!!!!

    I place my bet on Eunotosaurus for the time being.

    I wonder if the anapsid-like skull is the byproduct of some superossification development program associated with the development of the shell.

    That said, the completely anapsid Odontochelys has a rather weakly developped shell.

    That said, the recent redescription of the skull of Mesosaurus shows that M. had a temporal fenestra – which means that the temporal fenestrae in various “anapsids”/”parareptiles”/”proganosaurs” are homologous to ours, even if not to those of diapsids. That means turtles are secondarily anapsid either way! Madness! :-)

    What does developmental biology say about the development of the turtle skull?

    Not much.

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  19. 19. Heteromeles 8:58 am 06/10/2012

    Another fun physiological question: how does a turtle manage to get an erection without passing out? The issue here is that, with such a massive organ being erected by moving blood into it, that’s a substantial loss of blood supply for the other organs of the body, especially for the brain, which is at the highest end of the body during mating.

    If there isn’t an answer already, probably someone could get a grant to find out. After all, there might be a human medical application for the finding, as both hypertension and hypotension are major medical issues.

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  20. 20. JamesDavis 9:19 am 06/10/2012

    That is an exceptionally good article. I haven’t seen an article on SciAm that interesting and detailed since Jesse and his homosexual articles. Great job, Darren. I hope to read more great articles like this one coming from you.

    When you read articles like this, you may come to realize that we humans really did get cheated in life.

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  21. 21. John Harshman 10:36 am 06/10/2012

    What you actually need is a three-way death match among proponents of parareptile, sauropterygian, and archosaurian relationships. As a theropod neontologist, I naturally go for the third alternative.

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  22. 22. ChasCPeterson 11:16 am 06/10/2012

    jeez with the diapsid turtles.

    @comments #1 & 5: only pleurodires breathe with the cloacal bursae.

    I laughed twice:
    Hydraulic intromittent male sexual organs – a variety of popular, alternative names are available

    the overall form of the glans, varies from group to group (Zug 1966). Some of the configurations involved look terrifying; others look really terrifying.

    classic TetZool

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  23. 23. Eriorguez 7:04 pm 06/10/2012

    Aw, my name mentioned at Tet Zoo; feels real good, hope it gives a good impression when some possible employer googles my name…

    Anyway, from what I’ve been gathering, turtles are shaping up to be closer to archosaurs than to lepidosaurs, despite their lack of uric acid-based waste disposal (which I’d assume to be due to their ancestral marine lifestyle, at least for the modern species). The loss of fenestrae is quite odd, considering all other crown amniotans except the 20-odd species of crocodilians have this tendency to expose their braincase and fuse skull openings.

    Well, that’s a hunch, correct me if I’m wrong!

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  24. 24. Metridia 7:48 pm 06/10/2012

    Here are some papers on turtle skeleton ontogeny and development.

    Gilbert et al. 2001

    Burke 2005

    “The second phase of nuchal ossification involves the nuchal plate. This begins to form in embryos of CL1.8 cm. The nuchal plate forms as a loose lattice-work of bone, much like the pattern seen in the initial stages of ossification in the skull roofing bones. It begins in contact with the anterior-medial nuchal bar and extends laterally along the bar and posteriorly into the dermis above neural spines of the last two cervical vertebrae. This posterior extension of secondary dermal bone forms the main body of the nuchal and lies under the first vertebral scute. It will eventually form a suture with the first neural bone, which develops around the neural spine of the first thoracic vertebra.”

    Admittedly, there’s not a whole lot published; this would seem to be a great place for evo-devo to step in…

    Link to this
  25. 25. Jurassosaurus 8:13 pm 06/10/2012

    Turtles show up as archosaurs only under molecular phylogenies. Until I see some good morphology to back it up, I call B.S. (or long branch) on the whole thing.

    Link to this
  26. 26. Jerzy v. 3.0. 4:20 am 06/11/2012

    Picture 1 seems incorrect. On my pet red-eared slider I remember something umbrella-shaped with a row of pointed thorns along the rim. Also, folding and unfolding mechanism was quite interesting – the basal stalk moved out, then the flat top grew, and the spines seemed to move along the side a bit like halves of two chainsaws. Details were difficult to see – the male very rarely showed this outside the female, and it took just a second or two to extend and hide fully.

    Second Heteromeles about the mystery of not passing out!

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  27. 27. naishd 5:39 am 06/11/2012

    Thanks, everyone, for the many great comments and questions. This article has proved pretty popular in terms of bringing me hits: Tet Zoo ver 3 is currently in third place at Nature Blog Network (previously it was 9th or so), and this article has been getting over 10,000 hits per day. It’s just like old times (smiley). Tet Zoo ver 2, incidentally, has dropped off the radar at NBN, mostly because the new format (the one that erased all the thousands of comments) resulted in the removal of the NBN counter. Anyway…

    On the matter of how turtles manage not to pass out when erecting the penis, I don’t think that (as Heteromeles says) anyone has investigated this. It may be that comparatively little blood is required to inflate the vascular space in turtles. Or, is it that turtles have a comparatively large amount of blood? I haven’t looked into this, but I have read that the amount of blood in a sea turtle’s body is ‘average’ for an animal of its size (c. 7% of body mass – similar to that of humans). Waterfowl use lymph fluid to inflate the penis, but I don’t think there’s any indication that turtles do this.

    Turtle affinities: yes, I would love to write about this issue at some stage (did I mention that I’m currently working with Mike Lee?), and I also plan to cover parareptile diversity some time. Like a lot of people these days, I don’t mind the idea that turtles are close to (or within?) archosauromorphs, especially given the superficial turtlely-ness of some Triassic archosauromorphs, the discovery of a laterosphenoid in turtles, and the recovery in some studies of archosauromorph sauropterygians. So, the new molecular results from Crawford et al. (2012) are pretty encouraging.

    Darren

    Ref – -

    Crawford, N. G., Faircloth, B. C., McCormack, J. E., Brumfield, R. T., Winker, K. & Glenn T. C. 2012. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biology Letters doi: 10.1098/rsbl.2012.0331

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  28. 28. David Marjanović 6:25 am 06/11/2012

    Ontogeny backs up Odontochelys: the neural plates are not outgrowths of the vertebrae, but dermal bones that fuse to the vertebrae later (or not, as in O.); the costal plates are not outgrowths of the ribs, but metaplastic ossifications of the dermis that form on top of the ribs… a condition apparently shared by Eunotosaurus.

    the discovery of a laterosphenoid in turtles

    Very few fossils have been CT-scanned and are therefore known to actually lack laterosphenoids. I also wonder about homology to various pleurosphenoid stuff and whatnot.

    Crawford, N. G., Faircloth, B. C., McCormack, J. E., Brumfield, R. T., Winker, K. & Glenn T. C. 2012. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs.

    On the other hand, lepidosaurs in general and squamates in particular are famous for being very lax on conserving anything in the genome.

    The Amphibian Tree of Life (Frost et al. 2006) found the turtles outside Diapsida based on molecular data, but they used POY… a method to do the alignment and the phylogenetic analysis at the same time, which is a wonderful idea in theory but has been shown to fail a lot in practice.

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  29. 29. David Marjanović 6:27 am 06/11/2012

    did I mention that I’m currently working with Mike Lee?

    :-o You didn’t!

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  30. 30. Therizinosaurus 7:44 am 06/11/2012

    In response to both Jurassosaurus and Marjanovic-

    “Until I see some good morphology to back [any hypothesis] up, I call [uncertainty] on the whole thing.”

    http://theropoddatabase.blogspot.com/2011/06/rieppels-reptile-matrix-and-turtle.html

    Link to this
  31. 31. Tomasz Skawiński 7:59 am 06/11/2012

    If you follow these things, I would say that this name has rightfully won out over Dipsochelys dussumieri. Does anyone know if the ICZN has published a ruling yet?

    No – the case is still open for comments.

    Link to this
  32. 32. SafeLibraries 4:15 pm 06/11/2012

    An interesting example of convergent evolution, like marsupial frogs, but I learned about that in Scientific American as well. Thanks, SciAm!

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  33. 33. John Harshman 8:43 pm 06/11/2012

    Jurassosaurus:
    Turtles show up as archosaurs only under molecular phylogenies. Until I see some good morphology to back it up, I call B.S. (or long branch) on the whole thing.

    Wait — you’re willing to discount the great majority of the data? Why?

    Link to this
  34. 34. Jurassosaurus 12:27 am 06/12/2012

    Wait — you’re willing to discount the great majority of the data? Why?

    Molecular data has routinely put out questionable trees that have little to know cross-validation with morphological or fossil data (e.g., turtles as archosaurs, tuataras as archosaurs, iguanians as anguimorphs, and even birds being sister groups to mammals at one point). Molecular sequences are also subjected to high degrees of stochastic convergence (with only four base pairs to work with and millions of years for them to switch, the noise can flood out the signal). The allure of the molecular approach is that one can sequence thousands of base pairs and produce statistically rigorous results, but a large quantity of low quality data does not make for a better analysis.

    Link to this
  35. 35. naishd 4:02 am 06/12/2012

    Ok, I’m just gonna stand back and watch what happens now… this should be good! (smiley)

    Darren

    Link to this
  36. 36. David Černý 12:17 pm 06/12/2012

    Molecular data has routinely put out questionable trees that have little to know cross-validation with morphological or fossil data

    That only begs the question. You could as well say that it’s the morphological phylogenies that are questionable because they often contradict molecular data.

    Molecular sequences are also subjected to high degrees of stochastic convergence (with only four base pairs to work with and millions of years for them to switch, the noise can flood out the signal).

    Substitution saturation is a problem only for sequence analyses. It doesn’t affect rare genomic changes that have a much larger character state space – and at least one type of RCGs (microRNAs; Lyson et al. 2011) supports the diapsid position of turtles. (Although within Lepidosauromorpha instead of Archosauromorpha. The Crawford et al. paper suggests it’s an artifact of using small libraries of easily detectable miRNAs.)

    [...] and even birds being sister groups to mammals at one point

    But the Haematothermia hypothesis was first proposed by morphologists (Gardiner, Løvtrup, and of course Owen) on the basis of shared soft-tissue endothermy-related characters. Hedges et al. (1990) managed to support it with NJ and parsimony analyses of three different loci, but model-based methods and analyses using larger amounts of data did not corroborate the result.

    Refs:

    Hedges SB, Moberg KD, Maxson LR 1990 Tetrapod phylogeny inferred from 18S and 28S ribosomal RNA sequences and a review of the evidence for amniote relationships. Mol Biol Evol 7(6):607-633

    Lyson TR, Sperling EA, Heimberg AM, Gauthier JA, King BL, Peterson KJ 2011 MicroRNAs support a turtle + lizard clade. Biol Lett 8(1): 104–7

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  37. 37. John Harshman 4:15 pm 06/12/2012

    Substitution saturation is a problem only for sequence analyses.

    And, I might point out, a problem that can be detected and avoided in a number of ways: adding taxa to shorten branches, using sequences that evolve more slowly, using evolutionary models that take multiple hits into account.

    The idea that morphological characters have infinite characters states and thus that homoplasy is unlikely is pretty silly if you think about it. In fact the average morphological data set shows, if anything, a lower consistency index over its favored tree than does the average molecular data set.

    And of course morphological analyses have regularly put out questionable trees: monophyly of ratites (with kiwi as sister to the rest, at that) and polyphyly of Gavialidae being two that I’ve been involved with personally.

    All data have potential analysis problems. Morphology, like molecular data, is not privileged in this regard. And quantity has a quality all its own. We’ve learned more about phylogeny from 30 years or so (being generous) of molecular analyses than in 45 years or so of morphological cladistics. Much of this is due to the recent availability of masses of sequence data. Whales are artiodactyls, and we knew that even before there were fossil astragali to “confirm”. Flamingos and grebes are sister taxa, despite the inability of morphology to do more than provide a handful of post hoc characters.

    As methods of analysis have matured, and as more data have become available, weird results like guinea pigs not being rodents and birds not being diapsids have receded, except in the minds of those who prefer excuses to ignore most of the data.

    End of rant.

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  38. 38. vdinets 2:14 am 06/14/2012

    John: if you mean the position of false gharials, behavioral data strongly supports them being crocs rather than gharials. Beyond reasonable doubt, in my opinion, although I might be biased because the data is mine :-)

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  39. 39. John Harshman 12:07 pm 06/14/2012

    vdinets:

    I mean the positions of both Gavialis and Tomistoma. Molecular data universally and conclusively show that they are sister taxa of each other and are together the sister taxon of Crocodylus/Osteolaemus/Mecistops. If your behavioral data strongly support something else, you will have to explain the discrepancy. I just don’t see how you can ignore it. Some of the data are mine, but after many papers on the subject by many authors, only a small fraction thereof.

    And a hand-wave in the direction of long branch attraction isn’t an explanation. (I may be doing you a disservice there, but it’s a common excuse and a lame one.)

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  40. 40. vdinets 3:12 pm 06/14/2012

    John: It would be better if you explained the discrepancy, because (a) you are better qualified to do so since I am not an expert on molecular analysis, and (b) molecular data contradict both morphological and behavioral data, so you are now a minority :-)

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  41. 41. David Marjanović 5:04 pm 06/14/2012

    “Substitution saturation is a problem only for sequence analyses.”

    And, I might point out, a problem that can be detected and avoided in a number of ways: adding taxa to shorten branches,

    Only possible if there are taxa that can be added. In many such cases, there simply aren’t.

    using sequences that evolve more slowly,

    That’s possible, but doesn’t get rid of taxon-specific effects – both genome-wide and gene-specific ones.

    The idea that morphological characters have infinite characters states and thus that homoplasy is unlikely is pretty silly if you think about it.

    On this I agree. Most morphological characters have, or are generally treated as having, two states.

    Flamingos and grebes are sister taxa, despite the inability of morphology to do more than provide a handful of post hoc characters.

    AFAIK, morphology now supports Mirandornithes on its own, but I may be misremembering… and in any case I’m talking about analyses with way too few taxa here.

    weird results like guinea pigs not being rodents

    In hindsight, this was mice not coming out as rodents but being attracted to the long stem of Placentalia.

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  42. 42. David Černý 7:06 pm 06/14/2012

    Only possible if there are taxa that can be added. In many such cases, there simply aren’t.

    That’s possible, but doesn’t get rid of taxon-specific effects – both genome-wide and gene-specific ones.

    Still, it seems that in many cases, using advanced model-based methods (as opposed to parsimony) can overcome the saturation problem pretty well. Another technique that does help is RY-coding of the problematic sequences, which reduces the number of character states by coding nucleotides only as purines and pyrimidines. And if all that fails, one can shift focus from sequence data to RCGs such as retroposon insertions.

    AFAIK, morphology now supports Mirandornithes on its own, but I may be misremembering…

    It does: Mayr (2004) found 11 derived characters linking grebes and flamingos (two of them unique to these groups) and managed to recover Mirandornithes in a parsimony analysis even when gaviids were included. Manegold (2006) was able to find two more apomorphies. However, would we know/realize the importance of those characters if the relationship didn’t consistently emerge from molecular analyses? I think not, and John Harshman isn’t the only one who puts the word “confirmation” in scare quotes in such cases. The late Bradley Livezey (2011) called it “ambulance chasing” in his chapter in Living Dinosaurs; he explicitly criticized Mayr in this regard. I generally like the way Mayr supports molecular phylogenies with morphological data (it seems to be the only way to get the placement of fossil taxa right), but I can understand Livezey’s sentiment as well.

    Refs:

    Livezey BC 2011 Progress and obstacles in the phylogenetics of modern birds. 117–45 in Dyke GJ, Kaiser G, eds. Living Dinosaurs: The Evolutionary History of Modern Birds. London: John Wiley and Sons

    Manegold A 2006 Two additional synapomorphies of grebes Podicipedidae and flamingos Phoenicopteridae. Acta Ornithol 41(1): 79–82

    Mayr G 2004 Morphological evidence for sister group relationship between flamingos (Aves: Phoenicopteridae) and grebes (Podicipedidae). Zool J Linn Soc 140(2): 157–69

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  43. 43. John Harshman 9:29 am 06/15/2012

    vdinets:

    I’m afraid the discrepancy can’t be explained by examining the molecular data. They’re just too easy to analyze and too consistent for any other explanation than phylogeny to work. Have you considered mapping your data onto the molecular tree? Perhaps there’s some hidden signal there.

    I have tried a bit of explanation. There is for example a strong secondary signal in Brochu’s morphological data. See Harshman et al. 2003 and Gatesy et al. 2003. If there’s something more recent looking at this signal I have missed it.

    And thanks for putting a smiley at the end of your comment on “a minority”.

    Gatesy, J., G. Amato, M. Norell, R. DeSalle, and C. Hayashi. 2003. Combined support for wholesale taxic atavism in gavialine crocodylians. Systematic Biology 52:403-422.

    Harshman, J., C. J. Huddleston, J. Bollback, T. M. Parsons, and M. J. Braun. 2003. True and false gharials: A nuclear gene phylogeny of Crocodylia. Systematic Biology 52:386-402.

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  44. 44. vdinets 7:07 pm 06/15/2012

    John: the behavior I was looking at – the long-distance signaling – is otherwise consistent with phylogeny. What I got was Gavialis being totally different from everybody else. All others use the same signals, although Tomistoma and all crocs use them in different arrangements than gators and caimans.
    The only way to make it not contradict the molecular data is to say that Tomistoma is very conservative while Gavialis is outstandingly modified. But that would be tough to explain, considering that their lifestyle is fairly similar. There could be some unknown adventures in Gavialis’ past, of course…

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  45. 45. John Harshman 8:14 pm 06/15/2012

    So all you’re saying is that Gavialis has some autapomorphies. That isn’t inconsistent with any phylogenetic placement whatsoever; that is, your observations are irrelevant to phylogeny. Unless you are invoking some kind of behavioral clock, which it appears you are. I find that argument exceedingly dubious.

    Which is less likely: that Gavialis has experienced some episodes of rapid behavioral evolution, or that every one of some dozens of independently assorting genes (I have lost count at this point) each independently tells an identical but incorrect story?

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  46. 46. vdinets 11:32 pm 06/15/2012

    John: it’s not just “some” autapomorphies. Signaling behavior is conserved extremely well in other crocodilians: crocs and gators still have very similar and mutually intelligible “languages”. Gavialis, on the other hand, would have to have lost the entire repertoire, and then evolve a new one, with new signals having the same functions. It has replaced the so-called HOTA posture with snout-up posture (similar in appearance, but used very differently), all long-distance sounds (roars, headslaps, infrasound) with unique “bonk” sounds, and all short-distance sounds (hisses and growls) with “buzzing”, which is also unique. At the same time, Tomistoma, which has similar lifestyle, has typical croc repertoire. I find this very difficult to explain.

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  47. 47. vdinets 11:47 pm 06/15/2012

    Of course, there is one possibility: that soon after Tomistoma had split from the common ancestor of Crocodylus, Mecistops and Osteolaemus, that common ancestor was somehow subjected to radiation or some other mutagenic influence, which didn’t change its phenotype much, but made its genes look so different from those of both “gharials”. I wonder if a simple population bottleneck (or a few of those) could have that effect.

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  48. 48. John Harshman 9:12 am 06/16/2012

    vdinets: You have to look at all the data, not just your behavioral data in isolation. No matter where it goes in phylogeny, apparently the signaling behavior of Gavialis is highly autapomorphic. Its position on the tree doesn’t affect this conclusion. You have no basis, from your data, for concluding anything about phylogeny, except your opinion that the rapid evolution should have occurred on a common branch uniting the two gharials rather than on the true gharial’s branch. What reason is there for that opinion?

    On the other hand, just take a little look at the molecular data. No, a weird long branch for crocodylids doesn’t appear in the data, and that can’t explain the tree topology. And if there were a long branch, the crocodylids would be attracted to the root, and there would be a clade of gavialids and alligatorids. There is no alternative explanation, and it’s long past time people realized this. Densmore’s first paper on this subject was in 1983, and the ensuing 30 years have only strengthened his conclusion. But still we get posts like yours. Why?

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  49. 49. David Marjanović 5:34 pm 06/16/2012

    Still, it seems that in many cases, using advanced model-based methods (as opposed to parsimony) can overcome the saturation problem pretty well.

    Oh, sure. But then it sometimes crashes headfirst into heterotachy, which is no problem for simple parsimony at all.

    And if all that fails, one can shift focus from sequence data to RCGs such as retroposon insertions.

    That’s “molecular morphology”. It’s not sequence data, it’s presence and absence.

    However, would we know/realize the importance of those characters if the relationship didn’t consistently emerge from molecular analyses?

    Maybe we would, if a halfway adequate morphological analysis of neornithean phylogeny had ever been done. No such thing has ever been done; it’s just too much work (probably like several PhD theses).

    Livezey & Zusi made a rather pathetic attempt, and the people I talked to about this at this week’s SAPE meeting all talk about “horrible” issues with coding. Also, there are way too few fossils in that matrix.

    The late Bradley Livezey (2011) called it “ambulance chasing” in his chapter in Living Dinosaurs; he explicitly criticized Mayr in this regard.

    It’s apparently still better than what Livezey himself did.

    There is for example a strong secondary signal in Brochu’s morphological data.

    Brochu’s student had a tantalizing poster on this at last year’s SVP meeting.

    So all you’re saying is that Gavialis has some autapomorphies. That isn’t inconsistent with any phylogenetic placement whatsoever; that is, your observations are irrelevant to phylogeny. Unless you are invoking some kind of behavioral clock, which it appears you are. I find that argument exceedingly dubious.

    So do I. I don’t see why behavioral characters should be weighted more than other characters.

    Besides, if the current interpretations of the fossil record are any good, the last common ancestor of Gavialis and Tomistoma lived in the Cretaceous even if they’re each other’s closest extant relatives. A lot can happen in 70 million years.

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  50. 50. vdinets 8:24 pm 06/16/2012

    John: probably because Tomistoma looks like a fairly typical piscivorous croc, while Gavialis looks so strikingly different? And if the two are sister species, such differential rates of phenotype evolution beg explanation.

    David: I am not saying that behavioral characters should be weighted more than other characters. But they are an independent data set, and they do match phylogeny well elsewhere. Of course, a lot can happen in 70 million years, but why did it all happen only to Gavialis and not to Tomistoma?

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  51. 51. John Harshman 11:55 pm 06/16/2012

    Brochu’s student had a tantalizing poster on this at last year’s SVP meeting.

    Tell me more. Is there a published abstract?

    Besides, if the current interpretations of the fossil record are any good, the last common ancestor of Gavialis and Tomistoma lived in the Cretaceous even if they’re each other’s closest extant relatives.

    I don’t see how that can be true, given the branch lengths and topology of the molecular tree, unless you push, for example, Alligator way farther into the Cretaceous (at least), and that doesn’t seem credible. So I’m guessing that some of those Cretaceous gavialids are not.

    And if the two are sister species, such differential rates of phenotype evolution beg explanation.

    Indeed they do, and somebody should get on it. As a first step, you should map some characters onto the molecular tree.

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  52. 52. vdinets 1:30 am 06/17/2012

    Well, I tried mapping signaling characters on the tree. There are zero changes between Tomistoma and other crocs, two changes at the base of Alligatoridae, the reversal of one of these changes in Melanosuchus and Paleosuchus (probably independently, due to lower population density compared to Alligator and Caiman), one more change at the base of Alligator, and seven changes on the way to Gavialis. I think croc signaling is the ancestral form, because it is slightly simpler than Alligatorid signaling. If you accept that Gavialis is a sister taxon of Tomistoma, it means that Gavialis completely replaced all signals, and lost infrasound, which is highly effective in its habitat and should be conserved better than in most other taxa. It just doesn’t make sense.

    But if you assume Gavialis to be the earliest branch, than everything plots beautifully, with crocs+gators evolving their signaling system after the split, and the common ancestor having only something very basic. Sorry if this is difficult to follow, but I’m summarizing a 100-page thesis (available online at http://scholarlyrepository.miami.edu/oa_dissertations/570/).

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  53. 53. naishd 6:59 am 06/17/2012

    Vlad: interesting stuff. The fossil record suggests that early members of the gharial lineage indulged in a lot of transoceanic dispersal, and indeed that some/most/all taxa were denizens of marine habitats. In other words, gharials may have been far more ‘marine’ in habitus that the members of other surviving crocodilian lineages. I find it conceivable that this could help explain their many behavioural peculiarities. I will elaborate in an article some time.

    Darren

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  54. 54. David Černý 9:09 am 06/17/2012

    Oh, sure. But then it sometimes crashes headfirst into heterotachy, which is no problem for simple parsimony at all.

    I suppose you are referring to Kolaczkowski & Thornton (2004). However, subsequent papers attacked many of their conclusions: Spencer et al. (2005) demonstrated that you can pretty much close the performance gap by using more complex evolutionary models (K&T used only JC69 in their paper) and Gadagkar & Kumar (2005) showed that generally speaking, likelihood is superior to parsimony even under heterotachy, because cases of ML outperforming MP are more common than the opposite ones when the whole range of the heterotachous sites proportion is taken into account. Sure, none of this takes away from the fact that there are instances when MP fares better than ML, but then again, it’s hardly surprising that no method can outperform all others under all conditions.

    And the “no problem at all” part of your comment seems a bit exaggerated, too:

    “[...] there are 6 ways to assign two long and two short terminal edges on a labeled fourtaxon tree and 15 combinations of two different edge-length partitions. K&T described one such combination [...]. Over all combinations (fig. 1), there are nine where both standard likelihood and parsimony perform well. In two cases, both methods perform poorly, but parsimony does slightly better. In four cases, likelihood does better by roughly the same margin.”

    – Spencer et al. 2005:1161; the bolding is mine.

    That’s “molecular morphology”. It’s not sequence data, it’s presence and absence.

    In case of retroposons, it’s presence or absence at a given position, so it’s better viewed as one character with a huge number of character states (see, for example, Steel & Penny 2000).

    Livezey & Zusi made a rather pathetic attempt, and the people I talked to about this at this week’s SAPE meeting all talk about “horrible” issues with coding. Also, there are way too few fossils in that matrix.

    It’s apparently still better than what Livezey himself did.

    Sure — recovering a gruiform clade that includes cranes, eurypygiforms and seriemas (but not rails) in 2007 is downright insane. And the undersampling of fossils in the Livezey & Zusi matrix could well be intentional. The book chapter I’ve mentioned above is full of statements that express a rather strong dislike for fossils: “unjustified fascination attached to fossil taxa considered to be ‘mosaics’ of plesiomorphies and apomorphies”; “traditional folklore that elevates the perceived importance of fossils in establishing higher-order relationships”; “characters, not strata, inform [character state] polarities” (this one sounds quite reasonably, actually).

    However, I think he was right about one thing: post hoc search for morphological characters congruent with a molecular grouping does not constitute independent confirmation of that grouping. Of course, it doesn’t apply to everything Mayr does: his recent support for the molecular topology of Aequornithes in an analysis focused on pelagornithids was rather unexpected, for example.

    Refs:

    Gadagkar SR, Kumar S 2005 Maximum likelihood outperforms maximum parsimony even when evolutionary rates are heterotachous. Mol Biol Evol 22(11): 2139–41

    Kolaczkowski B, Thornton JW 2004 Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431(7011): 980–4

    Spencer M, Susko E, Roger AJ 2005 Likelihood, parsimony, and heterogeneous evolution. Mol Biol Evol 22(5): 1161–4

    Steel M, Penny D 2000 Parsimony, likelihood, and the role of models in molecular phylogenetics. Mol Biol Evol 17(6): 839–50

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  55. 55. John Harshman 9:28 am 06/17/2012

    Vdinets: If you assume that birds and mammals are sister taxa, a number of soft anatomy characters also plot beautifully. Focusing in a small suite of characters is however not a good way to do phylogenetics. You need to consider your characters in the context of other data.

    Anyway, you don’t consider the molecular tree at all in your dissertation. You consider two variant scenarios, but in each of them Gavialis is considered a priori to be the sister group of all other crocodylians. One of those variants, if unrooted, would be the same as the molecular tree, but you also polarize your characters a priori.

    I would also claim, in passing, that assuming a root at some hypothetical, primitive state is also poor practice. Given that there is no good outgroup for your characters, you should just go with an unrooted tree, or at least one in which polarity at the root is ambiguous. Autapomorphies should not have any influence on topology.

    I realize that phylogenetics is peripheral to your dissertation, but if you’re going to bring it up you need to seriously examine the data. You don’t even cite most of the relevant literature.

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  56. 56. vdinets 4:25 pm 06/17/2012

    John: but isn’t it right that all current trees, either morphology- or molecular-based, also find Gavialis to be a sister group to all other extant crocodilians (with a possible exception of Tomistoma, of course?)

    It is, of course, possible that Gavialis has the ancestral communication system. But it is highly unlikely, with its auditory bullae apparently used for producing “bonks”, and the ghara used in snout-up displays.

    Darren: I thought about this, and it does qualify for a possible explanation… but early Tomistominae are also found in coastal marine deposits (Piras, P.; Delfino, M.; Del Favero, L.; and Kotsakis, T. 2007. Phylogenetic position of the crocodylian Megadontosuchus arduini and tomistomine palaeobiogeography. Acta Palaeontologica Polonica 52 (2): 315–328.)

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  57. 57. David Marjanović 5:02 am 06/18/2012

    Tell me more. Is there a published abstract?

    I don’t think SVP meeting abstracts are published anymore, except to registered attendees. Are they? They’re definitely not printed anymore, except on demand.

    There wasn’t much in the poster; the key word is “heterochrony”.

    In other words, gharials may have been far more ‘marine’ in habitus that the members of other surviving crocodilian lineages. I find it conceivable that this could help explain their many behavioural peculiarities.

    …Indeed! Gavialis is the most aquatic extant crocodylian, isn’t it? If it secondarily lives in freshwater, and I’m sure it does, that should have lots of effects on its behavior.

    I suppose you are referring to Kolaczkowski & Thornton (2004). However, subsequent papers attacked many of their conclusions:

    Yes… I know that paper was only the start of a literature battle that doesn’t seem to have come to a definite conclusion, though I haven’t read most of it; I remember seeing papers from 2006 on this issue.

    But you’re definitely right that only using JC69 was not a good idea!!! I managed to overlook that that’s what Kolaczkowski & Thornton did; thanks for pointing it out.

    The book chapter I’ve mentioned above is full of statements that express a rather strong dislike for fossils: “unjustified fascination attached to fossil taxa considered to be ‘mosaics’ of plesiomorphies and apomorphies”;

    That’s right in some ways. Presbyornis is not a shorebird/duck mosaic, it’s deeply nested within Anseriformes and close to Anatidae; Juncitarsus is not a shorebird/flamingo mosaic, it’s almost a grebe/flamingo mosaic.

    “traditional folklore that elevates the perceived importance of fossils in establishing higher-order relationships”;

    Over what?

    “characters, not strata, inform [character state] polarities” (this one sounds quite reasonably, actually).

    It is. But then, it’s a strawman. Nobody has used stratigraphy to polarize characters in 20 years; polarization must be done by the outgroup.

    you also polarize your characters a priori.

    I would also claim, in passing, that assuming a root at some hypothetical, primitive state is also poor practice.

    That’s the same thing – and it’s very bad indeed. It assumes part of the conclusions!

    early Tomistominae are also found in coastal marine deposits

    …while gharials must have crossed oceans all the time, probably all the way to the Cretaceous Thoracosaurus.

    Link to this
  58. 58. John Harshman 10:35 am 06/18/2012

    but isn’t it right that all current trees, either morphology- or molecular-based, also find Gavialis to be a sister group to all other extant crocodilians (with a possible exception of Tomistoma, of course?)

    No, it most certainly is not right, and I have to say I’m slightly appalled by this mistaken notion of the literature. Molecular trees consistently find alligatorids to be the sister group of all other extant crocodilians. To get the molecular tree, just take the morphological tree and move Gavialis so it’s right next to Tomistoma. Leave Tomistoma where it is.

    And nobody is claiming that Gavialis has the ancestral communication system. You in fact have no good way of telling what the ancestral communication system is, but any character shared among alligatorids, crocodylids, and Tomistoma is likely to be primitive for crocodylians.

    Link to this
  59. 59. vdinets 12:39 pm 06/18/2012

    David: crocs have also crossed the Atlantic, so trans-ocean dispersal doesn’t automatically mean marine lifestyle.

    Note that loss of infrasound (absent in Gavialis) is the opposite of what you’d expect to see in a marine group. Indeed, Tomistoma and saltwater crocodile have given up vocal communication almost completely in favor of infrasound and headslaps.

    John: in this case, gators are the outgroup for rooting the croc-gharial tree, which means croc/Tomistoma condition is ancestral and Gavialis condition is derived. That is a bit strange (see the previous paragraph).

    There’s plenty of sources considering Gavialis to be an earlier split than gators. For example:

    Brochu, C. A. 2003. Phylogenetic approaches toward crocodylian history. Ann. Rev. E. Plan. Sci. 31: 357–397.

    Poe S (1996) Data set incongruence and the phylogeny of crocodilians. Syst Biol 45:393–414.

    Link to this
  60. 60. John Harshman 5:54 pm 06/18/2012

    Vdinets: I’m achieving some level of frustration here. Yes, there are sources that consider Gavialis the sister group of all other crocodylians. That was never an issue. They’re all based on morphology alone, and most of them are in fact Chris Brochu’s publications. (Not that he’s a voice in the wilderness; he’s just prolific.) Poe, on the other hand, found the same topology I’m arguing for, on the basis of a combined morphological/molecular analysis, so your citation of his paper is mistaken.

    You may find it hard to explain your data given the molecular tree, but that doesn’t mean you can avoid or ignore that tree. Evolution isn’t necessarily easy to explain. Hypotheses must conform to reality, though, and by this point, given the amount of data, it’s pernicious to deny that the “molecular tree” reflects the reality of crocodylian phylogeny. It’s a source of serious annoyance to me that some scientists still reject that tree after 30 years of evidence, just because the evidence is primarily molecular.

    The similar situations with the flamingo-grebe clade and ratite polyphyly also annoy me. There is in fact plenty to annoy me in the world.

    Link to this
  61. 61. naishd 6:17 pm 06/18/2012

    With reference to the mention of Chris Brochu above (comment 60): just to be fair, Chris has always made clear in his publications that morphology and molecules sometimes produce conflicting trees, that combined data is the way to go, and that reliance on one data set is unwise. Indeed, several of Chris’s papers feature combined-character phylogenies, the conclusion being that gharials are within Crocodylidae (not outside the croc + gator clade) and close to Tomistoma.

    Darren

    Link to this
  62. 62. vdinets 6:39 pm 06/18/2012

    John: I am not ignoring the molecular data. I am just saying that behavioral data strongly matches morphology and totally disagrees with molecular data. Personally, I would prefer all three sets to be in perfect agreement, so that we could all be happy and Tomistoma could be officially renamed “false crocodile”. But that’s not the case, and there’s nothing I can do about it :-(

    Link to this
  63. 63. John Harshman 8:52 pm 06/18/2012

    vdinets: In fact your data do not strongly match morphology, as they don’t map with any different result on either the morphological or molecular trees. Your data make no statement about tree topology unless you make questionable assumptions about character polarity or evolutionary rates.

    Darren: Could you cite Chris’s papers in which he does the combined data analyses and finds the molecular tree? I may have forgotten or missed something here. And I was definitely making no attempt to put down his work. Last we talked, which was some years ago, he was still favoring (provisionally, of course, as a scientist should) the morphological topology.

    Link to this
  64. 64. Jurassosaurus 10:55 pm 06/18/2012

    Regarding saturation

    And, I might point out, a problem that can be detected and avoided in a number of ways: adding taxa to shorten branches, using sequences that evolve more slowly, using evolutionary models that take multiple hits into account.

    All of these depend on the assumptions that the sequences are 1)evolving slowly and 2) have a constant mutation rate. Violations of these (and other) assumptions often results in very different trees (Black and Roehrdanz 1998, Song et al. 2010). Due to the large amount of data contained in each sequence all these questionable trees also wind up having strong statistical backing to them, essentially nullifying the use of standard statistical techniques in eliminating bad trees (Kumar et al. 2012).

    And of course morphological analyses have regularly put out questionable trees: monophyly of ratites (with kiwi as sister to the rest, at that) and polyphyly of Gavialidae being two that I’ve been involved with personally.

    I don’t know about the ratite tree, but the idea that Gavialidae is paraphyletic is strictly a molecular one. In fact (as the numerous posts below this original one have shown) it is one of the quintessential examples of molecular trees plotting out contentious results. The molecular position of Gavialis not only disagrees with the morphological data, but also the paleontological data as animals closer to Gavialis than Tomistoma are known from the late Cretaceous (Brochu 2004), rather than the Miocene or younger estimates given by molecular phylogenies. That behavioural repertoires seem to fall closer in line with the morphological and paleontological data would seem to be yet another case of disagreement (though I share everyone else’s caution regarding the phylogenetic utility of behaviour).

    We’ve learned more about phylogeny from 30 years or so (being generous) of molecular analyses than in 45 years or so of morphological cladistics.

    I completely disagree here. In the past 30 years I have seen molecular phylogenies throw a wrench in every major reptilian phylogeny (turtles, squamates and crocs). Rather than teach us more about the history of reptiles it seems to have just muddied the water. It also doesn’t help that many of these molecular topologies were published without any real thought as to how they would affect current views on relationships, evolution and distributions (in particular see Townsend et al. 2004, but also Hedges and Poling 1999).

    Hypotheses must conform to reality, though, and by this point, given the amount of data, it’s pernicious to deny that the “molecular tree” reflects the reality of crocodylian phylogeny.

    The problem with the molecular data is that it is only backed up by more molecular data. This is not conforming to reality, but rather a subset of reality. That the morphological data and the paleontological data agree with each other would seem to make that topology a better fit for what we think really happened.

    Worse yet is the position of turtles. Again molecular data backs molecular data, but disagrees with morphological data, paleontological data and embryological data. Given such a wide disagreement I am more willing to side with the preponderance of data that says turtles are something closer to basal reptiles/diapsids than to archosaurs.

    It’s a source of serious annoyance to me that some scientists still reject that tree after 30 years of evidence, just because the evidence is primarily molecular.

    I find it interesting that you even run into it that often since one of my biggest pet peeves in the field today is how every time a new molecular phylogeny gets proposed and it conflicts with the morphological data, the attitude of the authors are that the morphologists got it wrong. Then, to add insult to inury, the morphologists turn around and say: “Yeah, we probably did get it wrong.” There seems to be this persistent belief that since molecular phylogenies use DNA, and have a crap-tonne of data, they must be correct. Ironically the biggest criticisms of molecular methods have come from other molecular systematists (Hillis 1994, Wiens and Hollingsworth 2000, Rabosky 2010). Some, such as John Wiens, are supporters of adding morphological data into the matrix and seeing how it affects topology (Wiens 2005, 2010) vs. the more common trend of throwing morphological characters on a premade molecular tree.

    Believe it or not I do respect molecular methods and don’t want to throw the baby out with the bathwater. However I also feel that there is a persistent trend in systematics of assuming that molecular phylogenies are somehow etched in stone and thus infallible, resulting in fewer molecular phylogenies being tested than similar morphological phylogenies. It is this trend that I think is doing the largest disservice to the field.

    References

    Black, W.C., Roehrdanz, R.L. 1998. Mitochondrial Gene Order is Not Conserved in Arthropods: Prostriate and Metastriate Tick Mitochondrial Genomes. Mol.Biol.Evol. Vol.15(12):1772-1785

    Brochu, C. 2004. A New Late Cretaceous Gavialoid Crocodylian from Eastern North America and the Phylogenetic Relationships of Thoracosaurs. JVP Vol.24(3):610-633

    Hedges, S.B. and Poling, L.L. 1999. A Molecular Phylogeny of Reptiles. Science 283:998-1001

    Hillis, D.M. 1994. Homology in Molecular Biology. in Hall, B.K. (ed). Homology: The Hierarchical Basis of Comparative Biology. Academic Press. San Diego, CA pps. 339-368

    Kumar, S., Filipski, A.J., Battistuzzi, F.U., Pond, S.L.K., Tamura, K. 2012. Statistics and Truth in Phylogenomics. Mol.Biol.Evol. Vol.29(2):457-472

    Rabosky, D.L. 2010. Extinction Rates should not be Estimated from Molecular Phylogenies. Evolution. Vol.64(6):1816-1824

    Song, H., Sheffield, N.C., Cameron, S.L., Miller, K.B., Whiting, M.F. 2010. When Phylogenetic Assumptions are Violated: Base Compositional Heterogenity and Among-Site Rate Variation in Beetle Mitochondrial Phylogenomics. Syst.Entemol. Vol.35:429-448

    Townsend, T.M., Larson, A., Louis, E., Macey, J.R. 2004. Molecular Phylogenetics of Squamata: The Position of Snakes, Amphisbaenians, and Dibamids, and the Root of the Squamate tree. Syst.Biol. Vol. 53:735–757

    Wiens J.J. 2005. Can Incomplete Taxa Rescue Phylogenetic Analyses from Long-Branch Attraction? Syst.Biol. Vol.54:731–742

    Wiens, J.J., Hollingsworth, B.D. 2000. War of the Iguanas: Conflicting Molecular and Morphologial Phylogenies and Long-Branche Attraction in Iguanid Lizards. Syst.Biol. Vol.49(1):143-159

    Wiens, J.J., Kuczynski, C.A., Townsend, T., Reeder, T.W., Mulcahy, D.G., Sites, J.W. 2010. Combining Phylogenomics and Fossils in Higher-Level Squamate Reptile Phylogeny: Molecular Data Change the Placement of Fossil Taxa. Syst.Biol. Vol.59(6):674-688

    Link to this
  65. 65. Jurassosaurus 11:01 pm 06/18/2012

    Darren – unless I missed a pub, Brochu’s still supports the morphological topology. He may be a proponent of total evidence models, but he has stated previously that their results are remarkably sensitive to the amount of data one way or the other. So when molecular data outweighs morphological data, then the molecular topology wins, but when the morphological data outweigh the molecular data then the morphological topology wins.

    See:

    Brochu, C.A. 2003. Phylogenetic Approaches to Crocodylian History. Annu.Rev.Earth Planet.Sci. Vol.31:357-397.

    Link to this
  66. 66. naishd 4:33 am 06/19/2012

    I have a very good memory when it comes to exchanges regarding stuff I’m interested in. Among the first technical papers I ever read on crocodylian relationships were those by Frey, Riess and Tarsitano on the position of gharials. Based on tail anatomy, they argued in 1989 that gharials are evidently outside the croc + gator clade. I found this pretty compelling. Some time about 1997 I corresponded with Chris Brochu about his then-new Leidyosuchus paper. I said that the morphological data convinced me that gharials were outside the croc + gator clade. His response was “Oddly enough, I’m not [convinced]“.

    Brochu & Densmore (2000) includes the sections ‘Where do the data sets agree?’ and ‘Where do the data sets clash?’. It described how the authors analysed the gharial problem using ND6 and cytb sequences: “In both cases, the position of Tomistoma was given high bootstrap support – a Gavialis-Tomistoma clade received 80% support with the bird outgroup.. ” (p. 5). Brochu (2000) also covers the gharial issue. Brochu says that fossils support a more ancient divergence than molecular data. Of course, 12 years ago is a long time, but you get the point.

    Darren

    Refs – -

    Brochu, C. A. 2000. Congruence between physiology, phylogenetics and the fossil record on crocodylian historical biogeography. In Grigg, G. C., Seebacher, F. & Franklin, C. E. (eds) Crocodilian Biology and Evolution. Surry Beatty & Sons (Chipping Norton, Aus.), pp. 9-28.

    - . & Densmore, L. D. 2000. Crocodile phylogenetics: a summary of current progress. In Grigg, G. C., Seebacher, F. & Franklin, C. E. (eds) Crocodilian Biology and Evolution. Surry Beatty & Sons (Chipping Norton, Aus.), pp. 3-8.

    Link to this
  67. 67. Dartian 6:38 am 06/19/2012

    Jurassosaurus:
    animals closer to Gavialis than Tomistoma are known from the late Cretaceous

    Maybe I’m just revealing my own ignorance here, but I have to ask: On the basis of what do we know that those Cretaceous thingies really are gharials? How confidently can we rule out the possibility that this is not just a case of convergent evolution?

    Link to this
  68. 68. Jurassosaurus 11:20 am 06/19/2012

    How confidently can we rule out the possibility that this is not just a case of convergent evolution?

    The possibility of convergence always exists and should be kept in mind, especially when many of the characters that unite the animals, are related to longirostry. That said, the typical signs of convergence (superficial resemblance with detailed structures differing) appears not to be there. For instance Gavialis is diagnosed by having an elongate rostrum composed of relatively short nasals that do not contact the premaxillae, and have no contribution to the naris. They are also characterized by having a mandibular symphysis that forms a broad “V” (vs. the constricted “V” seen in Tomistoma). These are characters shared in common with thoracosaurs too. There are also a couple of non-snout characters (braincase related characters) that help unite thoracosaurs with Gavialis too.

    In contrast, many of the features that were once used to unite thoracosaurs with Tomistoma (e.g., the “verticalized” braincase) turn out to be plesiomorphic features for a bunch of crocodylians, rather than synapomorphies.

    Ideally there would be postcranial characters added to this, but currently postcranial material is hard to find (or at least hasn’t been described) in a lot of these guys.

    Link to this
  69. 69. John Harshman 5:43 pm 06/19/2012

    All of these depend on the assumptions that the sequences are 1)evolving slowly and 2) have a constant mutation rate.

    I have no idea where you gained that impression. It’s certainly not a point made in any of your references. And it’s certainly wrong. But I will agree that if the assumptions of a model are violated one may get an incorrect tree. That much should be obvious. You have to show, however, that this is relevant to crocodylian phylogeny. What assumptions were violated in some particular analysis? (Or, really, all of them, since they all agree.) Song et al. mention compositional and site to site rate heterogeneity. The first is a rare problem, but there are models to deal with it if necessary. (In fact I did try such a model, and it made no difference.) The second is a common problem, and the models commonly used in analyses deal with it (and I used such a model in my analysis). I don’t have immediate access to Black & Roerdanz, but do you have reason to believe that whatever problems they talk about are operating in the current case?

    Or are you just looking for reasons to reject molecular data?

    The rest of the post seems to be a claim that one can’t believe molecular results unless they’re confirmed by morphology. Is this really your position? There is indeed a fairly strong secondary signal in Brochu’s data set that supports the molecular topology, but of course it’s a secondary signal. It’s interesting that the primary signal is strongly biased toward postcranial characters (or away from cranial characters, if you prefer) while the secondary signal is not. Nor is the secondary signal concentrated as a single node. Read Harshman et al. 2003 if you need details.

    Behavior doesn’t support the morphological tree. It’s equally compatible with either tree unless you make dubious assumptions about polarity and/or evolutionary rate. Are you willing to make those assumptions?

    The problem with the molecular data is that it is only backed up by more molecular data. This is not conforming to reality, but rather a subset of reality. That the morphological data and the paleontological data agree with each other would seem to make that topology a better fit for what we think really happened.

    But there’s so much molecular data. Again, this seems to be saying merely that you consider morphological data a priori superior. Why? Nor do I understand how the paleontological data can be separated from morphology. Are you talking about stratigraphy? That’s a weak argument at best.

    Harshman, J., C. J. Huddleston, J. Bollback, T. M. Parsons, and M. J. Braun. 2003. True and false gharials: A nuclear gene phylogeny of Crocodylia. Systematic Biology 52:386-402.

    I have no strong position on turtles, except that I would really like them to be archosaurs, just because it’s so cool. Can we agree that there’s good evidence they’re diapsids?

    Link to this
  70. 70. Dartian 12:35 am 06/20/2012

    Jurassosaurus: Thanks for the explanation.

    Follow-up question: In how many (extinct) lineages are gharial-like animals known to have independently evolved? Champsosaurs come to mind, but surely there are other examples?

    Link to this
  71. 71. Jurassosaurus 1:21 am 06/20/2012

    I have no idea where you gained that impression. It’s certainly not a point made in any of your references. And it’s certainly wrong

    The assumption of slowly evolving genes is, as far as I can tell, the main reason why conserved and “ultraconserved” regions are always chosen for molecular phylogenetics. If one can find a gene that seems to be evolving slowly, then the chances of it reaching saturation are less. Constant mutation rate is another standard assumption of all molecular models. I really doubt that this is news to you. To be clear here, I’m not talking about constant rate of mutation for each gene in each branch (i.e., the old molecular clock assumption), but the assumption that a gene that is evolving at a certain rate today, was evolving at that same rate 1, 10, 20, 50, or more million years ago in that line. The paper by Black and Roehrdanz. specifically cited a case where this assumption of conserved sequences was violated by empirical data (both for mitochondrial sequences and nuclear sequences) resulting in honeybees forming a well supported sister group relationship with ticks.

    You have to show, however, that this is relevant to crocodylian phylogeny. What assumptions were violated in some particular analysis? (Or, really, all of them, since they all agree.)

    This response was never meant to argue specifically for the position of gharials. That came up later in the comments. I was specifically stating examples of problems in molecular phylogenetics and why they give me cause for pause with each new tree.

    That said, briefly going over your paper, you aligned your c-myc data by eye? Given how my eyes start to blur things together at 100 base pairs, I’m not sure how you were able to accurately get 1100 base pairs to line up just right. Faulty alignments do adversely affect phylogenetic trees as Morrison and Ellis (1997) point out, so there could be a potential error there. You also used a fast evolving gene as your metric. I find that a strange choice since a faster evolving gene is more likely to hit saturation and increases the chance that stochastic change overwhelms the phylogenetic signal (Jeffroy et al 2006). You mentioned the indels being less susceptible to homoplasy than nucleotide substitutions, but if the indels are all from the rapidly evolving non-coding regions how much of a difference is that really going to make? You also only did two runs on your Bayesian analysis (default for Mr.Bayes). A dozen, or more runs may have helped to determine if you had actually reached the “true” tree and weren’t just stuck on the same island for both runs. And yeah, I know it’s easier to say “run a dozen analyses” than to actually do it, but runs of ten or more are encouraged for Bayesian analyses even if they might cause computer meltdowns (also something I’ve experienced).

    The rest of the post seems to be a claim that one can’t believe molecular results unless they’re confirmed by morphology. Is this really your position?

    Morphology, embryology, ecology, or paleontology. Just some other field from molecular systematics would make me trust the results more. I’ve seen too many wonky molecular trees for me to accept any on their own.

    There is indeed a fairly strong secondary signal in Brochu’s data set that supports the molecular topology, but of course it’s a secondary signal. It’s interesting that the primary signal is strongly biased toward postcranial characters (or away from cranial characters, if you prefer) while the secondary signal is not. Nor is the secondary signal concentrated as a single node. Read Harshman et al. 2003 if you need details.

    That there is a secondary signal is interesting. Brochu (2004) does address your concerns regarding potential secondary signals of the morphological tree, but even after recoding the two potentially confusing characters you cited, the results remained the same. So even If Tomistoma and Gavialis are each other’s closest relatives, it looks like they acquired their long snouts independently.

    But there’s so much molecular data.

    Yes, but unfortunately it seems to be to its detriment. Molecular systematics is in a unique position for biology. There are tonnes of data available allowing for robust statistical tests. Unfortunately this seems to have plagued molecular systematics with loads of type I errors in which many trees become statistically significant even when they disagree with each other (e.g., Jeffroy et al. 2006, Kumar et al. 2012), or are known to produce results that don’t pass the straight-face test (e.g., Black and Roehrdanz 1998).

    Nor do I understand how the paleontological data can be separated from morphology. Are you talking about stratigraphy? That’s a weak argument at best.

    Don’t be so willing to discount stratigraphy. Finding a canine skull in the Permian would be a big deal, and that’s just stratigraphy. Horner’s lab has fueled a resurgence in the importance of stratigraphy for dinosaur systematics (though they might place too much importance on it). Stratigraphy is important.

    Still I can understand the problem of separating paleontology from morphology. The finding of thoracosaurs as closer to Gavialis than Tomistoma was based on morphology. There are, however, other cases in which simple presence/absence would seem to work. For instance take a look at the examples that Darren cited in the Saltwater croc phylogeny entry. Molecular analyses suggest that Crocodylids started in Asia and then spread out towards Africa, but we have fossil data showing an extensive crop of crocodylids already in Africa during the time that they were “supposed” to be in Asia. There is very little morphology involved there (just enough to know it’s a crocodile).

    I have no strong position on turtles, except that I would really like them to be archosaurs, just because it’s so cool. Can we agree that there’s good evidence they’re diapsids?

    I think there is mostly good evidence that turtles are weirdos. That said I do tend to push more for the parareptile position, mostly for the same reasons as yourself. I think it would be cool to know that we have extant members of this ancient lineage.

    What would be really cool would be if turtles wound up as “dwarf pareiasaurs” as Lee has previously argued. Unfortunately I don’t think there is much evidence for that anymore.

    References

    Jeffroy, O., Brinkmann, H., Delsuc, F., Phillipe, H. 2006. Phylogenomics: The Beginning of Incongruence? Trends in Genetics. Vol.22(4):225-231

    Morrison, D.A., Ellis, J.T. 1997. Effects of Nucleotide Sequence Alignment on Phylogeny Estimation: A Case Study of 18S rDNAs of Apicomplexa. Mol.Biol.Evol. Vol.14(4):428-441

    The rest of the refs have been posted in previous comments.

    Link to this
  72. 72. Jurassosaurus 1:28 am 06/20/2012

    Dartian – I suspect Darren can probably give a more accurate list, but off the top of my head I can think of champsosaurs, pholidosaurs, thalattosaurs, various metriorhynchids, gavialoids/tomistomines (break that up as you see fit), spinosaurs (Suchomimus in particular) and various phytosaurs like Mystriosuchus (not sure how many times it was believed to evolved in these guys).

    Link to this
  73. 73. John Harshman 11:57 am 06/20/2012

    The assumption of slowly evolving genes is, as far as I can tell, the main reason why conserved and “ultraconserved” regions are always chosen for molecular phylogenetics.

    I have to suppose that you are not all that familiar with molecular phylogenetics. But you have at least one example before you (mine) that this isn’t true. Neutrally evolving sequences can be quite useful in phylogenetics. It all depends on how deep a divergence you want to look at. Crocodylians are a very shallow divergence — at least in terms of evolutionary change — compared to what you may be familiar with; certainly compared to the distances among arthropod classes, and in fact compared to the distances among avian orders.

    To be clear here, I’m not talking about constant rate of mutation for each gene in each branch (i.e., the old molecular clock assumption), but the assumption that a gene that is evolving at a certain rate today, was evolving at that same rate 1, 10, 20, 50, or more million years ago in that line.

    Even with the clarification, that isn’t a problem. One thing that could potentially cause a problem, which conceivably might be the subject of that paper I still can’t access, would be failure of an assumption current models do make: proportional rates among sites. There is no assumption that rates or even site-specific rates don’t change over time; but there is an assumption that slowly evolving sites remain slow relative to fast-evolving sites, i.e. that if the rate changes along a branch that it changes for all sites so as to keep the ratios of their rates constant. Is that what you’re trying to say?

    You comments on the cmyc data suggest to me that you have never actually looked at the data. Genetic distances are low enough to make alignment trivial. If you think there’s something wrong with the alignment you are free to change it and reanalyze, but I would be exceedingly surprised if it made any difference whatsoever.

    The fact that the Bayesian analysis came up with the same topology as all the other analyses should satisfy your doubts as to whether we had reached stability.

    You seem to be grasping at anything, no matter how irrelevant to the actual case, in order to cast doubt on the result. Do you do the same with morphological studies? If so, you must suppose that we know nothing about phylogeny. You really are granting a special status to morphological data, and again I ask why.

    Just some other field from molecular systematics would make me trust the results more. I’ve seen too many wonky molecular trees for me to accept any on their own.

    Have you ever seen a wonky morphological tree? And yet you accept morphological results without such confirmation. Really, the distinctions here are artificial. At bottom, it’s all genetic data, right? There’s no particular reason confirmation from, say, a set of cranial characters should be greater support than confirmation from an unlinked gene.

    More data is only a problem if it’s more bad data, i.e. data analyzed incorrectly. If you want to doubt the molecular results you have to show why the data are bad/analyzed incorrectly. Instead, you are tossing out generic objections that have nothing to do with the actual data. Some problems are easy to solve with sequence data; crocodylian relationships are one of those problems. Branch lengths are short but not too short; in fact the cmyc 3′ utr shows zero homoplasy on its most parsimonious tree. Try to make something of that.

    Molecular analyses suggest that Crocodylids started in Asia and then spread out towards Africa, but we have fossil data showing an extensive crop of crocodylids already in Africa during the time that they were “supposed” to be in Asia.

    This isn’t an argument about tree topology. It’s an argument about mapping of geography onto topology. That’s not a problem with the phylogenetics. It’s a problem with assumptions of range stability.

    Link to this
  74. 74. David E. 8:17 pm 10/12/2012

    How come none of you scientist types knows that the plural of penis is penes? (That’s two syllables, like axis, axes.)

    Link to this
  75. 75. naishd 6:20 am 10/13/2012

    David E: the plural term ‘penes’ might be in use, but ‘penises’ is not wrong; it’s an alternative.

    Darren

    Link to this
  76. 76. rock johny 1:08 am 08/15/2014

    Unless you happen to be a genius penius.

    Link to this

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