Merry Christmas, 11 by ~@Himmapaan on deviantART

Merry Christmas, 11 by ~Himmapaan on deviantART.

This has to be one of the most incredible pieces of palaeo-art, or even art I’ve ever laid my eyes upon!

Full credit for this delight goes to @himmapaan (link above) ❤

The image depicts what I presume is Parasaurolophus walkeri, infamously referred to as “Elvis” by Roland Tembo (the late Pete Postlethwaite) in Jurassic Park: The Lost World, a name coined by the bizarre head-gear this particular hadrosaur possessed.

As well as being an excellent image, it also appears quite anatomically correct: the derived tridactyl pes, a quadrupedal stance, heavy caudo-femoralis musculature, and er, two lateral bags of fruit and veg..

The two little dwarf-men things are the less well-known sympatric fossils also from the Dinosaur Park Formation – palaeontologists just don’t want anyone to know yet, as it blows current estimates for the origins of humans out of the water. This may or may not be true.

I’m certainly going to be requesting a copy of this, and perhaps some more of his fantastic work (also definitely worth checking out!). Raw talent.

Palaeontologists Don’t Always See Eye To Eye

Disclaimer: Apparently Carlsberg don’t write my titles..

Back in May 2011, a study was published in Science describing the application of sclerotic ring and orbital morphology in determining daily activity (diel) patterns in extinct archosaurs. Recently, a comment and counter-comment have been published, both with pretty critical rhetoric. I figured that as it appears to be causing a fuss, I’d try and summarise the discussion, and add a few comments here (you know, for the masses of people that read this blog..)

The initial study provides “concrete evidence” of Mesozoic “temporal niche partitioning”, a pretty important find, if indeed valid. Combined with data from extant analogues, the authors infer that the visual ecology of Mesozoic archosaurs was a critical driver in the evolution of diel activity patterns.

Now, seeing as the geological record doesn’t really go down to intra-daily resolution, to infer short-term ecological patterns in extinct archosaurs, we must rely on extrapolating signals from modern analogues, formally known as the ‘extant phylogenetic bracket’ approach. This has been used successfully in many aspects of palaeobiology, ranging from sauropodomorph feeding styles to flight evolution in avian theropods, and is an increasingly useful concept in reconstructing extinct ecological parameters based on the intrinsic link between form and function. This concept is rigorously applied by Schmitz and Motani (2011a) on a range of extinct archosaurs to track the link between orbital and scleral form, and visual function.

The basis of this study relies on the fact that in extant amniotes (avians, squamates and mammals), sclerotic and orbital morphology is adequate to discriminate between various functional guilds pertaining to diel activity patterns. Proxies used to describe total morphology are orbital length and the diameter of scleral ring. This is my first issue – based on these proxies, it becomes an assessment of size-function, not form-function (form is the total dimensionality resulting from size and shape). Given the fact that these are relatively simple shapes (ellipses, in two dimensions), it would not have been difficult to use a simple semi-landmark outline profile as a faithful basis for reconstruction, and then run the subsequent discriminant analyses with these data (i.e., a geometric morphometric approach). This would be much more informative in terms of the overall geometry of both the orbit and sclerotic ring.

As in all studies of functional ecomorphology, the ability to distinguish between genuine functional signals, and morphological similarity due to relatedness from common ancestry (i.e., phylogenetic covariance) is critical. The authors state that they compensate for this second factor using a time-calibrated phylogeny. This is fine, as the proxy they use for branch lengths (i.e., chronostratigraphic time) is currently almost the only metric for estimating phylogenetic distance, until someone formally publishes a phylogeny of extinct amniotes using, for example Bayesian methods (which provides estimations of phylogenetic distance), and including all of the species mentioned in the study. Thumbs up.

The only thing I really HATED about this study, is the following assertion: “Ecological niches previously occupied by non-avian dinosaurs are now filled by mammals”. Now, take the following definition of the ‘ecological niche’ from Wikipedia, “the relational position of a species…in its ecosystem to each other”. This implies that the ‘ecological niche’ is a relative spatio-temporal concept, and is firstly, flexible as a lineage develops, and secondly not something that can simply be switched between lineages, especially those as temporally disparate as extant mammals and extinct Mesozoic archosaurs.

Most of the rest of the article is taken up by describing similarities and differences between the extant and extinct species analysed, a summary of which is not required here. It is however, worth mentioning the other ecological parameters which the authors touch on, such as foraging time and metabolic rates. This is a nice touch, discussing how diel activity is a critical factor in assessing overall energy budgets in extinct archosaurs.

Ok, so on to the first response, or ‘technical comment’. This is mainly a critique of the novel discrimination method employed by Schmitz and Motani (2011a), with additional comments on the data and interpretation of the results. Hall et al. (2011) use the same data as the original study, and conduct a simpler method of analysis (a linear discriminant function analysis), which, actually doesn’t make a lot of sense. In the supplementary material provided with original study, all of the code is provided for meta-analysis or replication of the study, and was written explicitly for the data set used. So why not use it? The results of their analysis revealed a lot of ambiguity, with a lot of organisms (up to 80% in one group) being incorrectly classified within their a priori assigned groups. A total of 21% of the species were “misclassified” by the model employed. This is fair enough, but doesn’t really make sense when the method of analysis is effectively a simpler and less appropriate one than the one which is being questioned.

The second major point the authors make is that the theoretical and empirical basis is flawed, due to the assumption that “Mesozoic amniote activity patterns should conform to those of extant amniotes”, and due to the nature of taxon sampling “cannot be construed to represent a typical Mesozoic world and cannot be apportioned based on modern taxa”. Firstly, this second point is irrelevant, as it is the fact that the taxa used contain the relevant morphological structures that is of concern, not whether or not they represent a contiguous sample. Secondly, they question the use of extant analogues to infer ecological conditions in the past. Why not just say that the whole concept of comparative anatomy between extinct and extant organisms is flawed? They basically imply that the entire phylogenetic extant bracket approach is inappropriate here, as amniotes might not be comparable through time. This is not only a ridiculous statement to make (it’s employed in hundreds or thousands of other studies rather successfully), and again is irrelevant – the point is that the orbit and sclerotic rings are still present (and homologous) in all specimens analysed, and that its function is well understood.

Irrespective of these errors mentioned above, the article does have a couple of redeeming points. They concur with my earlier point that orbital diameter is a poor proxy (for axial eye diameter), due to the non-spherical nature of the structure, but fail to mention an alternative as suggested above. Secondly, they correctly point out that in the discriminant function ordination (in the supplementary data), many of the extinct organisms analysed fall outside the groupings in discriminant space (not “morphospace” as used), and thus may not be analogous in terms of activity patterns. Most of these species are actually the herbivorous archosaurs (such as ornithischians and non-theropod saurischians), which is an interesting point in itself. There may also a second meaning, that these exclusive species may represent more complex morphologies than any extant amniote, and are possibly more ecologically advanced. Maybe.

The counter-response (Schmitz and Motani, 2011b) offers no compromise in terms of what Hall et al. (2011) claim about the initial study. The authors respond with a rather messy discussion of discriminant analysis. They fail to mention what is probably the most important point however, in that group classification is assigned a priori to analysis, and it is this which controls the group dispersion structures. The various statistics mentioned simply measure the probability (or likelihood) of whether these group distributions are random or if there is some extrinsic underlying control. However, I have personally never conducted a discriminant analysis including prior probabilities, so cannot confidently comment further.

The authors respond to Hall et al. (2011)’s criticisms of the theoretical basis, by re-iterating that the concept of uniformitarianism is a sound logic for extrapolating ecological factors in extinct organisms. They then become a little hypocritical, stating that it is logical for themselves to use prior probabilities as a basis, but not for Hall et al. (2011) as it forces constraints on their analysis.

With regards to the herbivorous archosaurs that plot outside the extant amniote discriminant space (not “morphospace” again), the authors simply state that despite that Mesozoic archosaurs having larger eyes, they were able to be interpreted functionally still. Well, no not really. By definition there is nothing to compare them to. This is a pretty big issue with the main result of the study. I had a similar issue in my recent thesis, regarding comparative ‘traits’ in ornithopods and ruminants; the way to resolve it wasn’t to disregard different discriminant space occupations, but to consider the implications that in the terms of the particular features analysed, there was some temporal discontinuity that represented a distinct change in ecological function.

As the penultimate point, it is worth discussing the final paragraph of the counter-response: “Discriminant analysis of continuous morphological traits with explicit functional relevance provides a testable, quantitative model of ecomorphological inference” (my emphasis). In this context, how much sense does it make to take something that is by definition continuous, and attempt to place boundaries on it, that may or may not represent some functional category. Observe Figure S1 in the supplementary information: given the scatter of data, what is the purpose of trying to recover discrete categories, when clearly none exist? The nature of the data is continuous, therefore let the nature of the data interpretation be continuous. Any threshold designation between putative groupings will be arbitrary, and counter-intuitive. As well as bad practise.

As usual, I’m going to finish on a tangent. A lot of people are currently quite openly and very strongly questioning the relative value of peer-reviewed publication. These articles were all published in Science, which is one of the top journals in terms of impact factor. Now, with this strong discussion that is occurring post-publication, questioning both the theoretical and methodological basis and the strength of the data, what was the point in the pre-publication peer-review stage? Clearly, ‘they’ did not pick up on any of the discrepancies or flaws discussed above, and these were only highlighted once the study reached the attention of the academic public, who can and have contributed meaningfully to the study. Since initial publication, the value of this study has increased through the open critical discussion, not the publishers or the initial reviewers. This is how science should be conducted, and how scientific progression is optimised. Accordingly, it will be interesting to follow the progression of this study in terms of both study and reviewer success.

 

Merry Christmas in the mean time, and a Happy New Year to all three of my readers!

Fossils – So Much More Than Just Pretty Dead Things

What do fossils tell us? It’s an obvious question, commonly phrased as ‘What is the point in studying fossils?’, but often can be one of the more difficult ones to answer objectively. The most prominent reason, that I’m sure a lot of people will agree with, is that we want to know what ancient and often extinct organisms looked like. This promise of discovering the unknown is what captivates people from a young age, and often motivates them in to studying fossils as a profession. From fossils, we can infer ecological aspects such as behavioural interactions, feeding strategies, and predator-prey relationships, and how these factors all changed through time. Tracking and reconstructing the co-evolution of the Earth and its biota is one of the most magical and beautiful stories ever to be told.

However, fossils can provide so much more than just aesthetic pleasure. If this wasn’t so, it would make grant proposals incredibly difficult – people don’t usually like giving away money just so a fanatic can play with fossils all day. So, palaeontologists have developed numerous excuses to satisfy funding bodies, to show that studying fossils actually has some scientific value.

The real motive is going “WT*expletive deleted*????” Sheer curiosity. Then, this develops into seeing that there was a *expletive deleted*load of stuff that was WAY different – how did this work? What does this tell us about how stuff works today? Mallison (2011)

Following are additional reasons why the study of fossils is not only awesome, but also indispensible in our understanding of biological and geological evolution.

Lineage Reconstruction

This is perhaps the most important use that fossils have for evolutionary biologists and palaeontologists. While genetic analysis might tell you about the particular history of a gene or genome, or the genetic evolution of species or populations (there are key fundamental differences between gene-trees and species-trees, something which molecular systematists miss out A LOT), they tell you virtually nothing about the phenotypic, or morphological evolution within a lineage. We don’t have many fossilised genetic markers (except in exceptional circumstances from permafrost-preserved mammoths), and thus must default to morphological analysis when tracking lineage evolution. While methods do exist for estimating and modelling the temporal evolution of species with respect to their genetic make-up, these can never provide such solid evidence as fossils can in terms of reconstructing ancient organisms, and the evolutionary trajectories leading to what we see surrounding us today.

The next two points are largely based on cladistic methodology. For a nice summary of cladistics, it’s worth quickly checking the following Wikipedia entry here. Essentially, cladistic analysis is the primary method for reconstructing cladograms, or trees, that represent the systematic and hierarchical classification of organisms. Note, that cladograms are not to be confused with phylogenetic trees, in which explicit evolutionary trends are inferred (i.e., patterns of ancestor-descendant relationships).

Novel Extinct Morphologies

Cladistics is based on the analysis of characters, which are formally broken down into character states. A character is essentially an aspect of morphology which can be expressed as a number of mutually exclusive variables, or character states. This forms the basis for analysis of species’ relationships and homology assessment. An example of how this can be expressed is:

Maxilla, anterior process, length: shorter (0) or longer (1) than the posterior process (taken from Sereno, 2007)

Now, if you want to reconstruct the phylogeny of any extant group with extinct members using just living members of the group and using just morphology, then you would directly neglect the unique character combinations that fossil species exhibit. This is important because, as a general rule (there are exceptions) the more characters included in a cladistic analysis, the greater the resolution achieved. Fossils can also provide transitional morphologies between species and additional information in areas of low resolution, and therefore resolved relationships are more evolutionarily stringent. Missing out the morphological information contained within fossils constitutes a severe case of neglect, and also disregards one of the most important aspects of any evolutionary analysis: time.

Character Polarity

As shown above, characters are broken down into various character states representing variations of a particular aspect of morphology. One of the main goals of cladistic analysis is to resolve the sequence of evolutionary transformation of these particular character states. If we increase the complexity slightly to include three variables, the character becomes known as ‘multi-state’. Keeping in line with the example shown above, one possible character is:

Maxilla, anterior process, length: shorter (0), identical (1) or longer (2) than the posterior process

Note that this is a purely hypothetical example to illustrate the point. To ‘transform’ from one of these character states to an adjacent one (i.e., 0<->1 or 1<->2) it costs one ‘step’ with the implication that it costs more to transform from 0<->2, and must pass through a transitional stage, character state 1. This is known as character ordering, and represents the directionless sequence of evolutionary transformation. However, what we want to know is the direction of character state transformation, to tell if a particular character state is the derived (apomorphic) or primitive (plesiomorphic) condition. This is achieved by polarising characters, and is where fossils play their part. As fossils are explicitly related in terms of chronostratigraphic age, this can automatically impose an evolutionary trajectory on character state polarity (i.e., the older fossils have the plesiomorphic state). This can also be achieved by ‘rooting’ a cladogram through outgroup assignment, which is an a priori determination of the plesiomorphic conditions through fossils; this is actually explained quite nicely here. The main point is that fossils perform a critical role in inferring sequences of phenotypic evolution.

Sampling Diversity

Now, one thing I’m sure palaeontologists are tired of hearing over and over is that the fossil record is biased in numerous ways (i.e., regarding sampling biases). Numerous studies have recently been undertaken to overcome these apparent biases, the most recent and critical of which is Hannisdal and Peters (2011). This paper explains how many of the patterns of fossil diversity we observe during the Phanerozoic can be explained by covariation between ancient biotas, sedimentation rates, and Earth system dynamics (e.g., ocean redox). Thus fossils, and the way in which we interpret them, are proving to be influential in how we interpret the co-evolution of, for example, biochemical and tectonic patterns, and contiguous biota assemblages.

The fact remains that, yes, the fossil record is biased. But now we can compensate for and use it to nurture our understanding of geological processes in deep time. On the other hand, we have molecular systematists who consistently use the excuse of the ‘incomplete and biased’ nature of the fossil record to completely disregard the use of fossils, and assume that DNA-based analyses are adequate. This is actually pretty ironic, considering extant organisms (i.e., those we can extract DNA from) represent a single time slice containing a fraction of the total species that have existed on the Earth since life began, and is therefore the most biased sample of all. Hypocrisy, thy name is deoxyribonucleic acid. A recent example of this is Ericson (2011), in which fossils are neglected from the study entirely (with only a brief mention), thus compromising the accuracy of all results obtained (making inferences about Mesozoic palaeobiogeographic patterns without consulting the fossil record is pretty offensive). So, analysing and incorporating fossils into diversity analyses actually decreases relative sampling bias, and increases the empirical and theoretical validity of studies. Ignoring the fossil record for a biogeographical, phylogenetic, or any other evolutionary study is counter-productive, and pretty much blasphemy.

Breaking of Long Branches

Long branch attraction is a fairly common side-effect of genetic-based phylogenetic analysis, typically occurring in when invoking parsimony. It arises as the result of highly rapid divergence between multiple lineages, and due to the limitations of nucleotide substitution (i.e., four possible character states) can lead to misinterpretation of homoplastic sites (e.g., through reversals, parallelisms, or convergences of states) as homologous (orthologous) sites. This can lead to erroneous inferences about the evolutionary (i.e., topological) distances between lineages. Although using advanced modelling methods such as Maximum Likelihood or Bayesian analysis can partially resolve this issue with genetic data, fossils can also be used to ‘break up’ long branches by calibration against a particular lineage in deeper time (specifically in morphological analysis), or by providing information in areas of limited information, ultimately improving phylogenetic accuracy. This is another example of the limitations of molecular-based analyses, with analogous issues in morphological analysis being quite well understood and resolved (see Cobbett et al., 2007 for a nice discussion about including fossils in cladistic analysis).

Calibrating Molecular Phylogenies

Molecular phylogenies are becoming increasingly used to estimate divergence times of major clades and as the basis for assessing temporal dynamics in within- and between-group diversification. However, using site-substitution rates alone to estimate the temporal origin of a clade (i.e., a node) is a poor estimation, regardless of the complexity of the models employed. Therefore, fossils with a strongly supported or well-defined taxonomic status can be used to calibrate the minimum origins of a particular clade, in a strict spatio-temporal context. This bypasses several assumptions made by models, such as stochastic or constant rates of site substitution, and is therefore an invaluable tool for accurately reconstructing phylogenies. Accordingly, the integration of ‘metadata’ (such as stratigraphy, or relative or absolute ages) is essential in reconstructing accurate phylogenetic relationships. It can also reveal additional crucial factors, such as the rates of phenotypic evolution, and how particular functional characters or morphological domains covary through geological time.

The above examples are just several of the more significant reasons why studying fossils is crucial, and how upon further critical analysis can yield unparalleled detail about the evolutionary history of life on Earth. It is worth noting that, although there are drawbacks and advantages to studying either the fossil record or the genetic evolution of extant taxa, it is when both are integrated that a more complete picture of global evolution emerges. Fossils are prominent in this reconstruction based on the unequivocal increased accuracy gained, but possibly at the cost of decreased resolution, due to the incomplete, patchy and biased nature of the fossil record.

To finish, I’ll quickly mention the concept of uniformitarianism: “the present is the key to the past”. This may be, in many cases of natural processes, but the past is also key to unlocking how it is the present transpired, and furthermore, in predicting future patterns of biotic diversification. To neglect the fossil record is to discard the one solid piece of evidence that we have in understanding global biotic responses to very real scenarios such as global warming.

 

Further reading

Butler, R. J., Benson, R. B. J., Carrano, M. T., Mannion, P. D. and Upchurch, P. (2011) Sea level, dinosaur diversity and sampling biases: investigating the ‘common cause’ hypothesis in the terrestrial realm, Proceedings of the Royal Society, Biological Sciences, 278, 1165-1170

Cobbett, A., Wilkinson, M. and Wills, M. A. (2007) Fossils impact as hard as living taxa in parsimony analyses of morphology, Systematic Biology, 56(5), 753-766

Ericson, P. G. P. (2011) Evolution of terrestrial birds in three continents: biogeography and parallel radiations, Journal of Biogeography, doi:10.1111/j.1365-2699.2011.02650.x

Hannisdal, B. and Peters, S. E. (2011) Phanerozoic Earth system evolution and marine biodiversity, Nature, 334, 1121-1124

Sereno, P. C. (2007) Logical basis for morphological characters in phylogenetic analysis, Cladistics, 23(6), 565-587

An Introduction to Fossil Preservation

Recently, the UKAFH invited me to write an article for them on fossil preservation. What kind of palaeontologist would possibly decline! [excluding inverts – they don’t count]

This is just a nice basic guide to taphonomic processes, designed for people with limited knowledge of geology or palaeontology. Feedback, as always, is welcome! 🙂

 

 

Introduction

The fossil record is our one and only key to a physical understanding of ancient or extinct life. Over the years a wealth of fossil remains have been uncovered, ranging from the earliest microbial life to the largest eukaryotic animals, and from isotopic signatures to fragments of DNA. These remains of dead organisms are found in two major divisions: as body fossils, where an actual specimen is preserved in some form or as trace fossils, where a particular aspect of an organism’s life is preserved, typically as trackways or burrows.

Processes

The process of preservation is termed taphonomy, and can be broken down into three main stages: necrosis, biostratinomy and diagenesis. The death of an organism, necrosis, is the initial stage in preservation, and is related to either trauma or physiology. Biostratinomy refers to the processes from death to post-mortem burial, such as transportation, bacterial decay and potential scavenging. The time taken during this stage is a critical aspect of preservation likelihood. Finally, diagenesis refers to the processes relating to the transformation of sediments into rock, and organisms into fossils. The mode of preservation leading to what we see in rocks is determined at this point, through the interaction of the surrounding sediment chemistry and the recalcitrance of various tissues. During these three stages, numerous factors act to destroy fossils, including microbial decay, predation, and a multitude of biogeochemical processes. In order for a fossil to be preserved, at some point in the taphonomic cycle, one or more of these processes must be arrested. The degree to which taphonomic breakdown is prevented is directly proportional to the degree of preservation attained.

Modes of Preservation

Permineralisation or Petrifaction

This is the most common style whereby soluble minerals in the surrounding sediments and fluids are deposited within interstitial organic pore spaces, leading to a variety of styles of preservation. This is the most common preservation in most invertebrates, organic-walled microfossils and bones. Directly observable using various microscopic methods, this needs to be distinguished from recrystallization and dissolution processes to reconstruct the initial tissue structure.

Desiccation

The most infamous recent occurrence of desiccation-based preservation is the “dinosaur mummy” from Dakota, the aptly named, Dakota. This Upper Cretaceous hadrosaur preserves actual recrystallized tissue remains, including tendons and ligaments and the epidermal microstructure, in amazing detail. The carcass is thought to have undergone rapid burial on the periphery of a sandy river channel, enclosing it in an anoxic environment and significantly enhancing its preservation.

Tar

The La Brea Tar Pits in Los Angeles, California are renowned for the immaculate presence of a multitude of Pleistocene-age mammals. They are the products of crude oil seepage, with lighter hydrocarbon phases being siphoned off via fractionation until just sticky tar remains. The predominant hypothesis for the mass accumulations of fossils is that, once an animal was mired, it became the target for packs of predators, who ultimately met the same sticky fate as their intended prey. Little soft tissue is preserved, but the concentration of bones more than compensates. The bones are actually infused by the tar, turning them a dark brown colour. Smaller invertebrates as well as plant macro- and microfossils are also abundant here. The tar creates a completely anoxic environment in which little to no decay can occur.

Amber

Amber is the solidified remains of ancient tree sap. Organisms that are unlucky (or lucky?) enough to be preserved in amber create the most intricate and beautifully preserved fossils of all. Featuring prominently as John Hammond’s cane top in Jurassic Park, they deserve pride of place due to the exquisite detail typically preserved. The most famous deposit is the Eocene-age Baltic Amber, which has produced perfectly preserved plants, insects and even small vertebrates. Amber, like tar, entombs organisms within a completely anoxic environment, ceasing all decompositional processes.

Carbonisation

This process involves the conversion of organic tissues into a carbonaceous film or residue through either pyrolysis (i.e., thermochemical decomposition) or destructive distillation (anaerobic decomposition), usually as a result of low-grade regional metamorphism. It is the process that converts woody material into coal seams. Typical fossils found preserved like this are graptolites in shales, typically associated with scavenger-free deep-water anoxic environments, as well as marine vertebrate integument (e.g., in the Holzmaden Shale).

Permafrost

Infamous for the occasional Woolly mammoth occurrence in Alaska and Siberia. The conditions lock organisms, complete with integument and flesh, in time. DNA has even been extracted from several specimens and is incredibly useful in accurately retracing pachyderm lineages.

Volcanogenic

Classic examples where volcanic interaction has led to sites of exceptional taphonomy include the Mistaken Point Biota (Ediacaran, Newfoundland), and the Jehol Biota (Lower Cretaceous, China). The advantages of volcanogenic interaction are two-fold; firstly, they create toxic, anoxic environments, and are typically rapidly deposited creating the perfect preservational scenario. Secondly, they contain radioactive elements which can be used for high-precision radiometric dating, which can be applied by association to intercalated fossiliferous horizons. At the two mentioned sites, episodic ash falls capture and smother local fauna and flora. These are typically found interbedded with thin mudstones and shales, suggestion that they are lakeside communities mixed in with autochthonous benthic fauna. Fauna preserved associated with these ash deposits have a diagnostic opisthotonic neck posture, infamously depicted in the birds and avian theropods of the Jehol fauna, in the classic ‘angel pose’. This is possibly indicative of hypersaline or toxic waters as a cause of death.

Traces

The study of trace fossils is known as Ichnology. Trace fossils are the direct result of biological activity and have their own independent taxonomic system. This makes them extremely useful in reconstructing the behavioural palaeoecology of extinct organisms. They can represent anything from nesting sites, to anastomosing series of trackways, and can be preserved as either exogenic (on the surface of a fabric) or endogenic (made within sediments). The preservation potential for trace fossils is typically a function of grain size and depositional facies.

Geological Biases

The fossil record is an incredibly biased sample of ancient ecosystems. Scientists estimate that only 15% of the composite species in an ecosystem are typically preserved, and of these, most are those with ‘hard parts’ (e.g., shells, cuticle, bone). There are also biases reflecting the depositional environment (e.g., fluvial, lacustrine, marine, aeolian, volcanogenic), and amount of rock sampled, amongst others, which recently scientists have begun to unravel in the hopes of better determining the controls on preservation through deep geological time, and the effect this has on our understanding of the fossil record and diversity dynamics.

Lagerstätte

Occasionally, palaeontologists are fortunate enough to come across sites of exceptional preservation known as Lagerstätten (German for ‘storage place’). These represent snapshots in time, and come into two flavours: Konservat-Lagerstätten and Konzentrat-Lagerstätten. The former represents an accumulation of fossils where the detail preserved is on an incredibly intricate level, such that ‘soft parts’ are visible, even to the molecular level. The best known examples of these include the Burgess Shale (Cambrian, Canadian Rockies), and the Jehol Biota (Lower Cretaceous, China). Here, preservation of articulated elements, original labile soft tissues, unaltered mineral compositions and orientations, and even intracellular structure can be preserved, indicating the early termination of diagenetic processes or that early mineralisation sufficiently outpaced degradation. Konzentrat-Lagerstätte, on the other hand, represent unusually high concentrations of fossils, typically representing an in situ community. A classic example of this is the Morrison Formation bone bed (Late Jurassic, North America). Deposits like these typically represent mass mortality events such as flooding.

Recent Advances

Until recently, most fossils were interpreted in terms of their macroscopic preservation features. However, with technological advances such as the increasingly commonly used computed-tomography (CT) scanning and scanning-electron microscopy (SEM), sophisticated details about micro-scale preservation in numerous fossils are being recovered. Accordingly, palaeontologists are uncovering more about macro- and micro-scale physical features, as well as physiological, cellular and even sub-cellular processes.

Further Reading

Allison, P. A. and Bottjer, D. J. (2011) Taphonomy: process and bias through time, second edition, New York: Springer

Nudds, J. and Selden, P. (2008) Fossil-Lagerstätten, Geology Today, 24(4), 153-158

Schweitzer, M. H., Avci, R., Collier, T. and Goodwin, M. B. (2008) Microscopic, chemical and molecular methods for examining fossil preservation, Comptes Rendus Palevol, 7, 159-184

Upchurch, P., Mannion, P. D., Benson, R. B. J., Butler, R. J. & Carrano, M. T. (2011, in press). Geological and anthropogenic controls on the sampling of the terrestrial fossil record: a case study from the Dinosauria. In: Comparing the Geological and Fossil Records: Implications for Biodiversity Studies, McGowan, A. J. and Smith, A. B. (eds). Geological Society, London, Special Publication 358: 209-240

What defines a ‘trait’ in ecology? Part 1 of ‘Ecologists Please Try Harder’

If anyone reading this personally knows me, they will be able to tell you that one of my pet peeves at the moment revolves around the definitions of commonly used words in ecology such as ‘trait’ and ‘niche’. This article is going to focus on what is specifically meant by a ‘trait’, in an ecological sense. I’m going to save ecological niche for another day – in my first article for this blog, I briefly expressed the variable contexts in which it is commonly used, or misused, using a postgraduate conference as an example.

The background behind the desire to do this stems from, in my experience, an apparent inability for anyone to quantify or empirically validate what a trait really is. During my recent MSc, I posed the simple question ‘what is a trait?’ to most of the class, and also to a couple of the professors that taught us (not naming any names, but they both loved insects). Surprisingly, not a single one of them could answer, despite the diversity of associated backgrounds (geologists, palaeontologists, zoologists, entomologists, botanists, etc.)! Considering the rampant use of this term in the literature as, I feel some clarity needs to be given to the precise definition, or concept, of the trait.

To begin with a few simple definitions, typing “define: trait” into Google gave the initial [relevant] definition of “A genetically determined characteristic”; so essentially, any aspect of a phenotype. A definition further down is “Qualities that make one organism different from another”. Further down still, another is “A particular aspect of the phenotype that can be measured or observed directly”. As an sub-ironic side note, Word listed ‘trait’ as a synonym of aspect when I checked during writing this.. Anyway, the second of these is pretty subjective, and also incredibly broad, and is fairly similar to the inverse of homology. The third is an extension of the first, but still provides no resolution in terms of scale – it implies that any aspect of the phenotype, from hair length to number of skin cells on middle finger, can be used as a trait. Similarly, any process, be it chemical, biological or mechanical (or any combination thereof) can also be regarded as a trait. What about in geometric morphometrics? A program I wanted to use recently regarded every single x and y of each co-ordinate a single trait (that was 200 ‘traits’ representing a 2D snout profile!!)

So, if a trait is just any aspect of phenotype, then what is its heuristic value? Morphology is typically broken down into characters and character states, focussed around the concept of biological homology and primarily for use in cladistics. It can also be broken down into functional domains, such as the regions of the axial skeleton (e.g., cervical, dorsal, sacral and caudal vertebrae, and the skull). This has an inherent value, in that each domain has individual parameters that define it, be it from something simple like vertebral count, to the variable strains induced on the skeletal elements during locomotion.

Recently, I discussed the concept of traits briefly with a PhD student at the University of Leicester. He mentioned that the value of the term to ecologists is that it is all-encompassing. I disagree, and, like with homology, a formally well-defined concept, believe that the value of the term lies in the precision of the definition and what it describes. To have a scientific value, the term must imply something that is transparent, and comparable on the necessary levels. I believe that the term ‘trait’ offers neither of these.

To look at occurrences of its academic use, I simply whacked ‘trait’ into Google Scholar, refining it to articles from 2011. It came up with quite a lot of irrelevant garbage, so the search was refined to ‘trait ecology’. Now you’re talking! Out of the host that were found, I selected just a few randomly to see how they used traits in their studies. Below is a list of the papers selected, and an attempt to disseminate what they mean by the term ‘trait’ in each particular and independent study. The references for each are below, and I can provide pdfs if necessary.

Cornelissen et al.

Leaf pH is used as a biochemical plant functional trait. Variation here is attributed to either a species’ genetic makeup or phenotypic plasticity, and additional contributing factors mentioned are seasonal variation and environmentally controlled physiological variability. So there are a host of potential parameters that control trait variation – how do you infer how much of a governing influence one or numerous ones are? We see no empirical or theoretical background again for deciding what a trait is and what is not, and what controls putative trait variation.

Coulson et al.

Utilises a model that classes populations as “fluctuating distributions of phenotypic traits and genotypes”. I think they just use body mass here, combined with genotype in influencing reproductive success. Body mass results from the complex interaction of biological parameters (e.g., feeding efficiency), and climate, as well as latitude and plausibly Cope’s Rule, amongst others. Why not just use ‘body mass’? Why use ‘trait’..? It’s taking something well-defined and quantitative, and dumping it in a bucket with every other aspect of phenotype.

Diniz-Filho et al.

In point 3 of their Abstract (or Summary?!), the first two mentions of traits are immediately followed by “(i.e., body mass)”. They then mention that they were going to deconstruct this trait into phylogenetic and specific components and that each one of these would be a trait too. You can probably see where this is going.. (edit: they actually used ‘niche’ and ‘trait’ in the same sentence at one point. More atrocious than climate change denial).

Hérault et al.

Utilises 17 functional traits (i.e., related to leaf economics, stem economics and life history) in plants, including maximum height, specific leaf area (leaf area/leaf mass), seed mass, wood density. Now, I don’t know about you guys, but when you measure an aspect of morphology, isn’t that called morphometrics? Each one of these putative quantitative traits  is based on a different metric that may or not be independent of each other, and may or may not be related to intrinsic biology as opposed to extrinsic factors.

Laughlin et al.

Functional traits synonymised with “phenotypic properties”, in that traits are environmentally reactive and predict performance. How do you quantify this? Is a trait such as body/leaf/seed mass not the influence of many other smaller-scale parameters? It is a gross over-simplification of phenotypic complexity that closer inspection through character analysis can reveal.

Pavoine et al.

These guys/gals actually mention traits in a phylogenetic context. If you read the following paragraph, it’s pretty obvious that all they’ve done is replaced the word ‘morphology’ with ‘trait’.

“However, many approaches have conflated phylogenetic information with trait values (particularly where trait information is unavailable), relying on the underlying hypothesis that closely related species are more likely to have similar traits than distantly related species. Studies that have combined the analyses of traits with phylogenies, in a context of community assembly, have revealed that convergence in trait states can occur among unrelated species.”

At this point, they haven’t mentioned what a trait is, or what aspects they are actually studying. Within their analyses, they treat all ‘traits’ as independent, and despite calibrating for phylogeny, means that the study (imo) is methodologically flawed.

Piqueray et al.

Identification of traits that increase the likelihood that species will support an extinction debt. The authors actually make a note of what they define to be a trait, the first time I have ever came across this: “a measurable characteristic of an organism”. This only serves to convey the subjective basis of trait acquisition and analysis; I mean, c’mon, measurable characteristic? Not vague at all.. The authors describe another trait following this, “only present in grazed grasslands” (page 1622). This is not a characteristic, it’s a characteristic of a characteristic. The point again is, if a trait can physically be anything, then what is it’s value as a concept?

Raes et al.

Molecular trait variation in the context of ecosystem processes in microbial communities using environmental shotgun sequencing (i.e., metagenomics). Lateral gene transfer and species dispersal are described as functional traits in a spatial context, or so it seems.

“[investigate] the factors influencing functional dispersal (defined here as the functional effects of species dispersal as well as horizontal gene transfer and phage-mediated gene flow), i.e., the movement of functional traits through geographical space” (page 2).

 

Note that I’m not saying any of these studies are wrong or flawed due to their use of ‘traits’, I’m simply highlighting the unconstrained variability in which the term is used. There are more references, but they really all follow the same routine. Given the amount of work and debate that goes into understanding and defining the concept of homology, why hasn’t the same attention and scrutiny been given to an almost equally used and valuable concept?

Following this and considering that the term is used so widely, if it is removed or modified, how would people cope? I don’t think it needs strict removal, more just stringently defining as a concept. It needs to be transparent, so that people know when to apply it, and when not to, and also what it can be specifically applied to. It needs to be refined to exclude and include certain factors, and each factor should be purely independent (as in homology). The problem possibly stems from the fact that ‘trait’ has a purely denotative definition; the “any phenotypic aspect” bit. But the connotative definition is unconstrained and poorly defined. I’d like to think that the above examples illustrate this, as if I say ‘trait’ to any of the authors, it is likely they will consider the subjective definition as applies to their personal research.

Also, what of missing data? Phylogeneticists shiver at the very thought of it when constructing a character matrix. So what of missing trait information? If you are regressing twenty ‘traits’ against environmental variables to find a correlation, are you sure that this is enough to capture the entire suite of functionally coupled parameters? Analogous to genomic sequencing, you have to use every piece of available data to reconstruct your trees – the same reasoning should apply to trait data. Except we’ve already seen that a trait is any aspect of phenotype, so it might take a while..

Penultimate point: using body mass as a functional trait is something I’m extremely sceptical about. The opening clause of the abstract from Cooper and Purvis (2010) is probably the most important quote pertaining to this: “Body size correlates with virtually every aspect of species biology” . This is with respect to mammals, and the most significant result of their study is that body mass evolution “has been influenced by a complex interplay among geography, climate, and history”. This should be a strong warning to studies using body mass as a functional trait.

Finally, note that all of the above references are in biological journals. Palaeontologists seem to be doing fine without using ‘traits’! (not that I’m at all biased) Oh, and only a couple of them did any form of phylogenetic regression (i.e., to account for ‘trait’ covariation resulting from common ancestry), so..yeah. But then, I probably don’t get it, not exactly being an expert in the field..

Clarity, constructive comments, and sarcasm would be appreciated.

 

Edit: http://www.onto-med.de/obml/ws2011/obml2011report.pdf#page=15 Just found this. For additional reading, looks useful. Enjoy! I’m off to play Skyrim..

 

References

Cornelissen, J. H. C., Sibma, F., Van Logtestijn, R. S. P., Broekman, R. A. and Thompson, K. (2011) Leaf pH as a plant trait: species-driven rather than soil-driven variation, Functional Ecology, 25, 449-455

Cooper, N. and Purvis, A. (2010) Body size evolution in mammals: complexity in tempo and mode, The American Naturalist, 175(6)

Coulson, T., MacNulty, D. R., Stahler, D. R., vonHoldt, B., Wayne, R. K. and Smith, D. W. (2011) Modelling effects of environmental change on wolf population dynamics, trait evolution, and life history, Science, 334, 1275-1278

Diniz-Filho, J. A. F., Cianciaruso, M. V., Rangel, T. F. and Bini, L. M. (2011) Eigenvector estimation of phylogenetic and functional diversity, Functional Ecology, 25, 735-744

Hérault, B., Bachelot, B., Poorter, L., Rossi, V., Bongers, F., Chave, J., Paine C. E. T., Wagner, F. and Baralato, C. (2011) Functional traits shape ontogenetic growth trajectories of rain forest tree species, Journal of Ecology, 99, 1431-1440

Laughlin, D. C., Fulé, P. Z., Huffman, D. W., Crouse, J. and Laliberté, E. (2011) Climatic constraints on trait-based forest assembly, Journal of Ecology, 99, 1489-1499

Pavoine, S., Vela, E., Gachet, S., Bélair, G. and Bonsall, M. B. (2011) Linking patterns in phylogeny, traits, abiotic variables and space: a novel approach to linking environmental filtering and plant community assembly,  Journal of Ecology, 99, 165-175

Piqueray, J., Bisteau, E., Cristifoli, S., Palm, R., Poschlod, P. and Mahy, G. (2011) Plant species extinction debt in a temperate biodiversity hotspot: community, species and functional trait approaches, Biological Conservation, 144, 1619-1629

Raes, J., Letunic, I., Yamada, T., Jensen, L. J. and Bork, P. (2011) Toward molecular trait-based ecology through integration of biogeochemical geographical and metagenomic data, Molecular Systems Biology, 7, doi:10.1038/msb.2011.6