Green Tea and Velociraptors

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