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Ars comparandi: “molecular convergence” versus “functional homology”

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Physicists measure—biologists compare. This statement is of course oversimplified, but describes a principal difference between the two sciences (ignoring the fact that also measuring is a kind of comparison, because… Click to show full abstract

Physicists measure—biologists compare. This statement is of course oversimplified, but describes a principal difference between the two sciences (ignoring the fact that also measuring is a kind of comparison, because objects or phenomena are compared to a unit of measurement). Life is manifold, and in order to describe this complexity, one has to filter out the particularities of a given life form, and to focus on its general features. To tell apart what is Bparticular^ and what is Bgeneral^ appears far from trivial, though. The art of comparing requires not only a thorough understanding, how a life form is structured, but also insight into development, physiology, interactions with the environment, and evolutionary history. Morphological similarity may lead astray, when these facets are ignored, because similar selective pressures may channel evolution towards similar shapes, a phenomenon termed as convergence. A meaningful biological comparison requires, however, that the similarity stems from a common origin, i.e. that the life forms to be compared show true homologies. In practice, it can be very tricky, to distinguish homology and convergence, especially in life forms where the evolutionary relationships are not clear. As a guideline, comparative morphology employs three classical criteria to validate homology (Remane 1971): continuity, specific quality and position. The ample use of sequence information (of both nucleotide and protein sequences) has meanwhile made life much easier, because sequence similarity immediately allows to infer on phylogenetic relationship, a methodological twist that has not only diluted the term homology, but also has undermined the ars comparandi: to sequence the genome of an organism appears more convenient than to deal with all the anatomical and functional details of its body structure. In this context, it is often overlooked that also molecular phylogenies are based upon homology criteria: When we align two sequences, we use the criterion of position to define corresponding base pairs or amino acid residues, which is not so different from the procedure used to tell that a bird wing is homologous to a human arm. To tell that two proteins are corresponding and therefore informative for a comparison, we use presence, order and sequence motifs of characteristic domains, which is nothing else than applying the criterion of specific quality. And in order to validate a common origin of two sequences, we use the criterion of continuity by including into our phylogenetic tree numerous sequences from related organisms. As long as we compare sequences from closely related life forms, this approach works neatly. Things become more challenging, when we have to work without the continuity criterion, for instance, because our life form is isolated, or because we want to conduct higher-level comparisons of more distant life forms. Here, the term Bhomology^ can readily turn into something void of any meaning (Zuckerkandl 1987). More than ever, molecular data have to be integrated with a deeper understanding of the functional context, in which a life form develops and survives. Three contributions to the current issue show how such knowledge on functional and cellular details helps to understand molecular data. The small heterocyclic molecule indole-acetic acid was originally predicted as transportable growth signal (auxin) in plants by the work of Darwin, Cholodny, Went and many others. Since its molecular identification by Thimann, auxin belongs to the most intensively studied plant signals, because it is transported directionally, providing a flow that orients and guides plant development from the first division of the zygote. The work by Borchers et al. (2018) adds a seemingly exotic new facet to our understanding of auxin as directional cue for plant development: These authors investigate a rotational movement of leaves in the model plant Arabidopsis thaliana. Although organ movements in sessile organisms may appear as nothing more than a playful detail of Nature, such twisting Handling Editor: Peter Nick

Keywords: ars comparandi; homology; life form; life; life forms; convergence

Journal Title: Protoplasma
Year Published: 2018

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