Wednesday, 18 January 2017

The brains of cats

So 2017 begins on a high for publishing with another paper hot off the presses and long overdue:

Cuff AR, Stockey C, Goswami A, 2017. Endocranial morphology of the extinct North American lion (Panthera atrox). Brain, Behavior and Evolution. DOI: 10.1159/000454705.

To quickly catch everyone up, P. atrox is an extinct lion from North America (as the paper title suggests). The species evolved from a "cave" lion (P. spalaea) population from Eurasia that crossed the Bering Sea around 340,000 years ago. These lion populations in turn split from the lineage that gives rise to the modern lions 1.89 million years ago (Barnett et al., 2016).

Phylogeny of the lion species
A quick note, endocasts are the natural cast (the infilling) of the endocranium (the braincase). In mammals the brain almost entirely fills the cavity so brain and endocast are almost identical (which is why brain swelling is such a major health issues). Birds are similar with their brains filling most of their endocast, but most non-avian dinosaurs and crocodiles have large sinuses that take up large volumes of the endocranium. Prior to our study the only data for P. atrox was from casts of skulls, (where they infilled brain cases with material to produce a cast) carried out in 1932 (Merriam and Stock, 1932). The new study adds some more details to those casts, as well as some additional information on the inner ear (red in the figure below).

From Cuff et al., 2017. Fig. 1. Endocranial reconstruction of P. atrox in left lateral ( a ), right lateral ( b ), dorsal ( c ), and ventral ( d ) views. Anterior is toward the left in a, c, and d and toward the right in b . The endocast is rendered in blue, the inner ear in red, and the cranial nerves in yellow. CN II, optic nerve; CN V 1–3, trigeminal nerve (ophthalmic, maxillary, and mandibular branches); CN VII, facial nerve; CN VIII, vestibulocochlear nerve; CN IX, glossopharyngeal nerve; CN X, vagus nerve; CN XII, hypoglossal nerve; hy, hypophysis/pituitary; ob, olfactory bulb; ocx, olfactory cortex; pf, paraflocculus; v, vermis. Scale bar = 20 mm. The endocranial orientation in a and b is linked to the likely “alert” head posture
We also compared the morphology of the extinct North American lion to modern Asian/Asiatic lions (below).
From Cuff et al., 2017.Figure 2. Endocranial reconstruction of P. leo persica in A, left lateral; B, right lateral; C, dorsal; and D, ventral views. Anterior is toward the left in A, C, D and toward the right in B. The endocast is rendered in blue, the inner ear in red, and the cranial nerves in yellow.; CN II optic nerve; CN V1-3, trigeminal nerve (ophthalmic, maxillary and mandibular branches); CN VII facial nerve; CN VIII vestibulocochlear nerve; CN IX, glossopharyngeal nerve; CN X, vagus nerve; CN XII, hypoglossal nerve; hy, hypophysis/pituitary; ob, olfactory bulb; ocx, olfactory cortex; pf, paraflocculus; v, vermis. Scale bar = 20 mm. Endocranial orientation in A and B linked to the likely “alert” head posture. 
Overall the endocasts look fairly similar, but something that you might have noticed is how much more elongate the P. atrox brain looks relative to the modern lion (P. leo). There are some previously published 2D models of some extinct taxa (Radinsky, 1975), with the oldest species showing this similar "elongate" morphology. However, the morphology seen in P. leo where the forebrain sits further back on the hindbrain is more "folded" and was also seen in some of the extinct species (particularly the sabre-tooth cats). So we needed a way to quantify the elongate/folded brain morphology (linked to cephalic flexure), which ended up being a simple ratio of length of hindbrain not covered relative to total brain length (P. atrox and P. leo shown below):

Long line is total length, short line is "exposed" hindbrain not covered by the forebrain.
We however lacked information for many of the extant species on whether the elongate or folded brains were more common and if there were any patterns. Therefore we got hold of a bunch of CT scans from colleagues (Z.J. Tseng, C.Grohé, and J.J. Flynn), and Christopher Stockey (a summer student joined us from Imperial). Chris segmented endocasts from a wide range of extant taxa (see below).
From Cuff et al., 2017. Figure 3. Brain anatomy through Felidae. Proailurus, Pseudaelurus, Dinobastis and Smilodon are all modified from Radinsky[1975]. Phylogeny modified from Piras et al.[2013], total length 27Ma. All scale bars = 2cm.
The results are shown in the table below, with the species with the most elongate brain morphologies with the highest proportion "exposed". P. atrox has 18.6% exposed, whilst P. leo is only 5.9% exposed (actually the lowest we measured). Typically, as with all biology, there is a spectrum rather than a hard and fast rule about the elongation of the brain of felids. Just within the pantherines (Panthera spp. - the big cats) there is a large range in the level of folding. Most of the other living species of cats are fairly consistent in their levels elongation.

Species
Cerebrum and cerebellum length
“Exposed” cerebellum length
Proportion “exposed”
Dinobastis sp.*
0.0979
0.0095
0.097
Smilodon fatalis*
0.0923
0.0124
0.134
Pseudaelurus*
0.0677
0.0165
0.243
Neofelis nebulosi
0.0717
0.0168
0.235
Panthera tigris
0.0999
0.0104
0.104
Panthera pardus
0.0918
0.0160
0.175
Panthera atrox
0.0984
0.0183
0.186
Panthera leo
0.0905
0.0053
0.059
Pardofelis marmorata
0.0550
0.0078
0.142
Carcal aurata
0.0671
0.0093
0.139
Leopardus wiedii
0.0517
0.0065
0.125
Lynx rufus
0.0655
0.0106
0.163
Acinonyx jubatus
0.0697
0.0080
0.115
Puma concolor
0.0855
0.0131
0.154
Prionailurus viverrina
0.0623
0.0108
0.174
Felis silvestris
0.0499
0.0100
0.200
Proailurus*
0.0641
0.0141
0.220

What does this mean? Honestly I don't know. It's a weird quirk of felid morphology that deserves further study, so there is a project if anyone wants to collaborate.

Beyond the crazy brain shapes, what about their sizes? We measured the volume of the endocasts and multiplied it by standard brain tissue density (somewhere between 1.027 g/cm3 [Schröder, 1968] and 1.100 g/cm3 [Barber et al., 1970]). This was this compared to the body size to get a relative brain size.

From Cuff et al., 2017. Figure 4. Regression of log maximum brain mass against log body mass (both in kilograms) for Felidae.
Most cats are fairly similar in relative brain size, with P. atrox slightly above that expected for its body mass. In addition, the absolute brain size (both of this endocast and some of the other P. atrox measured in 1932) is higher than any other felid species measured to date. But what does that mean for the intelligence? Actually in cats there doesn't appear to be an obvious correlation between brain size and sociality with similarly "brainy" cats being capable of both solo living and group living so we cannot say if P. atrox lived in prides like its modern relatives.

References
Barber TEDW, Brockway JA, Higgins LS (1970): The density of tissues in and about the. Acta Neurol Scand 46: 85–92.

Barnett R, Shapiro B, Barnes I, Ho SY, Burger J, Yamaguchi N, et al. (2009): Phylogeography of lions (Panthera leo ssp.) reveals three distinct taxa and a late Pleistocene reduction in genetic diversity. Mol Ecol Apr;18:1668–1677.

Merriam JC, Stock C (1932): The Felidæ of Rancho La Brea. Washington, Carnegie Institute of Washington.

Radinsky L (1975): Evolution of the felid brain. Brain Behav Evol 11:214–254.

Schröder R (1968): Über das spezifische Gewicht des Hirngewebes in der Nachbarschaft von Tumoren. Aus dem Max-Planck-Institut fur Hirnforschung, Abteilung fur Tumor forschung und expirementelle Pathologie, und der Neurochirurgischen Universitiitsklinik, Koln. 

Saturday, 31 December 2016

Year in review 2016

2016 was best described as a busy year. It started incredibly well with 4 publications in the first four months starting off in January with my first publication on a fossil I found:

Halliday TJD, Cuff AR, Prasad GVR, Thanglemmoi MS, Goswami A, 2016. New record of Egertonia (Phyllodontidae, Elopiformes) from the Late Cretaceous of South India. Papers in Palaeontology. DOI: 10.1002/spp2.1040. Paper link, blog.


The following month the PhD student on the project, Marcela Randau, published the first of her papers on the vertebral column of cats:

Randau M, Goswami A, Hutchinson JR, Cuff AR, Pierce SE. 2016. Cryptic complexity in felid vertebral evolution: shape differentiation and allometry of the axial skeleton. Biological Journal of Linnean Society. DOI: 10.1111/zoj.12403. Paper link, blog.


The early part of they year would also involve various efforts in the field with different cat species as a student and I attempted to gather force plate data (with varying levels of success).


March was a slow publishing month, but April was to be a double whammy with both the papers on cat muscle scaling across the postcrania:

Cuff AR, Sparkes EL, Randau M, Pierce SE, Kitchener AR, Gosawmi A, Hutchinson JR, 2016. The scaling of postcranial muscles in cats (Felidae) I: forelimb, cervical and thoracic muscles. Journal of Anatomy 229, 128-141. Paper link, blog

Cuff AR, Sparkes EL,Randau M, Pierce SE, Kitchener AR, Gosawmi A, Hutchinson JR, 2016. The scaling of postcranial muscles in cats (Felidae) II: hindlimb and lumbosacral muscles. Journal of Anatomy 229, 142-152. Paper link, blog


Also in April I joined Anjali (as well as Ryan and Carla from the lab) on another trip to Argentina where we joined up with our Argentinian colleagues for continued explorations of the Salta area looking for more fossils. It was a largely unproductive trip in terms of finding many new fossil locales, but we did rule out large areas, revisited the site I discovered previously and found another very promising site. Hopefully Anjali is successful with a large grant that would allow for a longer term exploration of the area with a bigger crew.


April was to be the final month of publishing for a while, but in May my blog passed the 10,000 view mark (or at least as far as blogger's tally count goes) so at least that publishing kept going strong. 

At the end of June and into early July I attended the International Congress of Vertebrate Mophology - ICVM. It was another fabulous conference with an abundance of cool science. It made up for not being able to make SVP this year, the first time I haven't attended in 6 years. In years gone by I've heard stories of the attendees who haven't missed on in 40+ years. Guess that won't be me!

The summer would lead to publishing my two most popular blog posts of all times, the first on why extraordinary claims need extraordinary evidence (still surprised there haven't been many comments on it), and the second on some of my favourite figures from palaeontological papers. Both posts got over a thousand hits in their first month which no other posts before or since have matched.


August was a particularly crazy month as I was expecting to be unemployed when September got around. Applications had gone into various places with a fair few rejections before interview, one failed interview (although a friend got the job so can't be too upset about it), and eventually an interview at RVC which was successful in getting me three more months employment as a technician whilst searching for something longer term.

In September I started my technician role, and whilst filling in the paperwork to start was invited to interview for postdoc on John's massive European Research Council (ERC) grant looking at the evolution of pseudosuchians (the crocodile line), and dinosaurs in the Triassic. After a tricky interview and encountering what I now think is a brilliant question on who I would invite to a symposium about the project (although hated it at the time as I blanked on names), I would eventually be offered the position which I gladly accepted. I would be returning to dinosaurs in December, learning some new techniques, and having a couple more years at the RVC.

After a six month hiatus, October would bring the next publication with Marcela again publishing on felid vertebral columns and her kindly writing a blog post for me becoming the first guest blogger on my site.

Randau M, Cuff AR, Hutchinson JR, Pierce SE, Goswami A. 2016. Regional differentiation of felid vertebral column evolution: a study of 3D shape trajectories.Organisms, Diversity & Evolution
DOI 10.1007/s13127-016-0304-4. Paper link, blog

November would result in my paper on felid brains (in combination with Anjali and our summer student/Imperial Uni undergrad) being accepted, and at present it has a DOI, but we are awaiting proofs before it gets published fully. I was hoping it would be fully online before the end of the year to count as published in 2016 and take my final total up to 6 for the year but it has not made it. At the start of the year I had hoped for 7-10 papers to be published this year. The 2 papers in review (one should be accepted after this round), a few failed projects (like digital image correlation on cat bones) and collaborations that are completed from my end, but not submitted are where I fell short. All of these should add to the expectation of at least 5 more by the end of 2017.

Ultimately December would bring the start of my second postdoctorate on the ERC project (expect many, many posts over the next few years on it), as well as leaving the UK for a much needed 3 week break having not had time off since Easter and feeling exhausted from work.

Across the year I have been practicing what I preach in regards to reviewing papers, with 12 reviews completed for 5 papers across 6 journals (one I got for 2 different journals when it wasn't deemed suitable for the first journal). Somewhat crazily, I have accepted another review across the Christmas holidays, so will be reviewing another one early in 2017.

It has been another good year for me, although maybe not so much politically for science in the UK with Brexit threatening large amounts of funding and collaborations. It shall be interesting to see where things go and I live in the optimistic (and probably vain) hope that it is not the doom and gloom we all fear,

A final amazing figure for the year from an undergraduate research project at Leicester (and a great example of how to get students thinking about science at all levels). I have to say I have nothing to do with the research, but it is a fun studying into whether the satellite phone swallowed by the Spinosaurus in Jurassic Park 3 could really have been heard by the main characters.
Childs et al., 2016. Dinosaur in-dial-gestion. Journal of Physics Special Topics.
Fig 1. A rough model of the path travelled by the sound, with Z-values from the literature.
Happy New Years and best wishes to all for 2017!

Wednesday, 23 November 2016

The cat's backs - a guest post

Two papers recently have come out that I have been involved in, and am thankful to Marcela Randau (the primary author) for giving up time between finishing a PhD, postdoc hunting and preparing for lecturing to write this post. If anyone reads whatsinjohnsfreezer.com regularly, you will see an identical post there as Marcela, understandably, didn't have time to write two similar but different posts for us both as we clambered for her expertise in felid vertebral columns.

The cat’s back.
by Marcela Randau (m.randau@ucl.ac.uk)
It is often said that all cats are very similar in terms of their skeletal morphology (“a cat is a cat is a cat”). But is this really the case? It may be if only gross, qualitative anatomy is taken into consideration, i.e., if you just eyeball the skeletons of tigers and lions you might find yourself not knowing which one is which. But with huge advances in technology that allows for extracting detailed shape information off a structure (e.g., a skull) and for analysing this information (‘Geometric Morphometrics’), it has become more and more possible to distinguish between relatively similar forms – which may be from distinct species, separate sexes, or even just different populations of the same taxon.

And it is reasonable to think that cat skeletons might be a lot more different than what meets the eye, as for a lineage of apparently similarly built animals, with not that much variation in diet (all cats are hypercarnivores) there is substantial variation in body mass (over 300-fold just in living species!) and in ecology across cat species. From the cursorial cheetah to the arboreal clouded leopard, felids present a wide range of locomotory adaptations. Yes, all cats can climb, but some do it better than others: think lion versus margay (yes, they do descend trees head-first). As hypercarnivores, all cats are meat specialists, but they also change with regards to how big their prey is, with a general and sometimes-not-so-black-and-white three-tier classification into small, mixed and large prey specialists. The rule of thumb is ‘if you are lighter than ~20-25kg, hunt small stuff. If you are heavier than that, hunt BIG BIG things, much bigger than yourself. And if you are in the middle ground, hunt some small-ish things, some big-ish things, and things about your size. Well, -ish’ – their prey size preference has a lot to do with energetic constraints (have a look at Carbone et al. 1999; and Carbone et al. 2007, if you're interested in this). But the fun bit here is that form sometimes correlates quite strongly with function, so we should be able to find differences in some of their bones that carry this ecological signal.

Indeed, for a while now, we have known that the shape of the skull and limbs of felids can tell us a lot about how they move and how big their prey is (Meachen-Samuels and Van Valkenburgh 2009, 2009), but a large proportion of their skeleton has been largely ignored: we don’t know half as much about ecomorphology and evolution of the vertebral column. Well, it was time we changed this a bit! As the PhD student in the Leverhulme-funded ‘Walking the cat back’ (or more informally, “Team Cat”) project, I’ve spend a big chunk of my first two years travelling around the world (well, ok, mainly to several locations in the USA) carrying a heavy pellet case containing my working tool, a Microscribe, to collect 3-D landmarks (Fig. 1) across the presacral vertebral column of several cat species. And some of first results are just out! Check them out by reading our latest paper, “Regional differentiation of felid vertebral column evolution: a study of 3D shape trajectories” in the Organisms Diversity and Evolution journal (Randau, Cuff, et al. 2016).

Fig. 1: Different vertebral morphologies and their respective three-dimensional landmarks. Vertebral images are from CT scans of Acinonyx jubatus (Cheetah, USNM 520539).
Building from results based on our linear vertebral data from the beginning of the year (Randau, Goswami, et al. 2016), the 3-D vertebral coordinates carry a lot more information and we were able to describe how this complex shape-function relationship takes place throughout the axial skeleton (in cats at least) in much better detail than our prior study did. One of the difficulties in studying serial structures such as the vertebral column is that some clades present variation in vertebral count which makes it less straightforward to compare individual vertebrae or regions across species. However, mammals are relatively strongly constrained in vertebral count, and Felidae (cats; living and known fossils) show no variation at all, having 27 presacral vertebrae. So adaptation of the axial skeleton in mammals has been suggested to happen by modification of shape rather than changes in vertebral number.

Using a variety of geometric morphometric analyses, under a phylogenetically informative methodology, we have shown that there is clear shape and functional regionalisation across the vertebral column, with vertebrae forming clusters that share similar signal. Most interestingly, the big picture of these results is a neck region which is either very conservative in shape, or is under much stronger constraints preventing it from responding to direct evolutionary pressures, contrasting with the ‘posteriormost’ post-diaphragmatic tenth thoracic (T10) to last lumbar (L7) vertebral region, which show the strongest ecological correlations.

We were able to analyse shape change through functional vertebral regions, rather than individual vertebrae alone, by making a novel application of a technique called the ‘Phenotypic Trajectory Analysis’, and demonstrated that the direction of vertebral shape trajectories in the morphospace changes considerably between both prey size and locomotory ecomorphs in cats, but that the amount of change in each group was the same. It was again in this T10-L7 region that ecological groups differed the most in vertebral shape trajectories (Fig. 2)
Figure 2: Phenotypic trajectory analysis (PTA) of vertebrae in the T10 – L7 region grouped by prey size (A) and locomotory (B) categories.
So in the postcranial morphology of cats can be distinguished, changing its anatomy in order to accommodate the different lifestyles we see across species. But the distinct parts of this structure respond to selection differently. The next step is figuring out how that might happen and we are working on it.

While Team Cat continues to investigate other biomechanical and evolutionary aspects of postcranial morphology in this interesting family, we’ve been able to discuss some of these and other results in a recent outreach event organised by the University College of London Grant Museum of Zoology and The Royal Veterinary College. We called it “Wild Cats Uncovered: movement evolves”. Check how it went here: (https://blogs.ucl.ac.uk/museums/2016/11/17/cheetah-post-mortem/) and here (http://www.rvc.ac.uk/research/research-centres-and-facilities/structure-and-motion/news/wild-cats-uncovered), with even more pics here (https://www.flickr.com/photos/144824896@N07/sets/72157676695634065/ ).

References used here:
Carbone, C., Mace, G. M., Roberts, S. C., and Macdonald, D. W. 1999. Energetic constaints on the diet of terrestrial carnivores. Nature 402:286-288.
Carbone, C., Teacher, A., and Rowcliffe, J. M. 2007. The costs of carnivory. PLoS biology 5 (2):e22.
Meachen-Samuels, J. and Van Valkenburgh, B. 2009. Craniodental indicators of prey size preference in the Felidae. Biol J Linn Soc 96 (4):784-799.
———. 2009. Forelimb indicators of prey-size preference in the Felidae. Journal of morphology 270 (6):729-744.
Randau, M., Cuff, A. R., Hutchinson, J. R., Pierce, S. E., and Goswami, A. 2016. Regional differentiation of felid vertebral column evolution: a study of 3D shape trajectories. Organisms Diversity and Evolution Online First.
Randau, M., Goswami, A., Hutchinson, J. R., Cuff, A. R., and Pierce, S. E. 2016. Cryptic complexity in felid vertebral evolution: shape differentiation and allometry of the axial skeleton. Zoological Journal of the Linnean Society 178 (1):183-202.