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 Animals are both radially and bilaterally

symmetrical: Accommodating seemingly

mutually exclusive paradigmsG abor Holl o

Animal symmetry is a fundamentalissue in biology. The two main symme-tries that characterize the animal worldare radial and bilateral symmetry. Theterm radial symmetry indicates thatthe animal is symmetrical around itslongitudinal axis. This is the antero-

posterior axis of polarity in mostanimals, and the oral-aboral axis inCnidarians and Ctenophores. Themembers of this latter phylum showbiradial symmetry with two planes of rotational symmetry. Bilateral symme-try is created when a second axis – thedorsoventral axis – also forms, per-pendicular to the anteroposterior axis.The process is due to the asymmetricalexpression of developmental genesalong this axis.

The phylogenetic relationship be-

tween the twosymmetries has long beena major question in biology. Accordingto the classical view, bilateral symmetry arose from radial symmetry (e.g. [1]).This view has become largely outdated.For example, in the case of Cnidaria –animals traditionally grouped withRadiata – it is known that the radialbody, which also contains bilaterally symmetrical elements, is organized by acomplex genome including severalbilaterian gene orthologs (e.g. [2, 3]).For this reason, it has been proposedthat Cnidarians be considered originally 

bilaterally symmetrical animals [4, 5].What is more, it also has been ques-

tioned whether truly radially symmetri-cal animals even exist or existed [5].

Axial patterning has been a focus of interest among developmental biolo-gists for many years. An abundance of data on the molecular mechanisms of axial patterning in Bilaterians, Cnidar-

ians, Poriferan larvae, and Ctenophoreshas accumulated in the past decades.However, although the genetic back-ground of the organization of axialpolarity is becoming ever clearer, thescientific community has not reached atrue consensus regarding the conflictingphylogenetic relationship of the twosymmetries. I think the reason for this ischiefly that our judgement on animalbody symmetry is too abstract, and isinfluenced by our love of categorization.It should be recognized that in most

cases, no clear and convenient symme-try type can be assigned to an animal.Do the bilaterally symmetrical internalstructures in the otherwise radial cni-darian body make it bilateral? Does theclearly cylindrical body form of anearthworm make it radially symmetri-cal, or is it the setae and the pairedinternal – even radially symmetric –organs that count?

In recent years, our understandingof the molecular background of theorganization of animal form has deep-ened significantly. It is now known that

the formation of the different body partsin the diverse phases of animal devel-opment is orchestrated by successively activated gene regulatory networks(GRNs; [6–9]). The expression of thediverse genes during development iscontrolled by regulatory DNA sequen-ces. These are activated by transcriptionfactors, each of which affects multiplegenes. The sum of the interactionsbetween regulatory genes forms a generegulatory network. It is also known

that the evolution of animal formoccurs mostly through the functionalremodeling of GRNs. This happensmainly via changes in the cis-regulatory modules that determine the expressionof regulatory genes [6, 7, 10], hencerewiring the GRNs [6, 9, 10]. It is

important to note that the geneticlinkages between the mosaically-acting,body-part-specific, GRN subcircuits aremore prone to evolutionary changethan their internal structures [9], thusensuring a marked modularity in thestructure of the developmental genebattery [6–9]. An important conse-quence of this modular structure is thatin the same body plan, sub-plans of different evolutionary age may bepresent [7–9]. Another inherent charac-teristic of the GRNs is their hierarchical

nature [6–9]. The GRN modules deter-mining phylum- and superphylum levelcharacteristics (named “kernels”; [6])reside at the core of developmentalprogrammes (top of the GRN hierarchy):they control major aspects of the body plan, and they are very stable overevolutionary time, being the mostslowly changing GRN subunits. How-ever, the GRN modules that are respon-sible for lower taxonomical levelproperties are activated at more termi-nal stages of development (lower levelsof theGRN hierarchy), and are subject to

more rapid evolutionary change[6, 7, 9].So in this context, the determination of symmetry axes in the overall body planis simply a characteristic that is con-trolled by slowly changing GRN mod-ules, whereas morphological features of minor anatomical structures are proba-bly established by generally more rap-idly evolving GRN subcircuits (althoughsome subcircuits low down in the GRNhierarchy may be very ancient [8, 9],further emphasizing the mosaic nature

DOI 10.1002/bies.201400089

Department of General Psychology, Institute of 

Psychology, University of Debrecen, Debrecen,

Hungary

Corresponding author:

Gabor Hollo

E-mail: hollo.gabor@arts.unideb.hu

www.bioessays-journal.com   1Bioessays 36: 0000–0000,   2014 WILEY Periodicals, Inc.

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8/10/2019 BioEssays Volume 36 Issue 9 2014 [Doi 10.1002%2Fbies.201400089] Holló, Gábor -- Animals Are Both Radially an…

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of the developmental GRNs). However,if we look at the animal world, fromCnidarians to   Homo, we can see thateither radial or bilateral symmetry may showup both in the overall body plan aswell as in smaller units of the body.Thus, on the basis of our current

knowledge of developmental genetics,we cannot necessarily say that any symmetry would be intrinsically of ahigher order than the other, nor that oneof them would be more ancient inevolutionary terms.

If we consider the relationshipbetween the symmetry of the body and that of its parts to be a questionof a diverse timing of separate GRNs,and symmetry as a feature strongly influenced by function, it seems reason-able that a genome benefits frommaintaining the potential to form both

symmetries (Fig. 1). I think the animalworld could be seen from a novel angle:as genomes that are able to build eitherbilateral or radial anatomical structures.In this context, the old question caneasily be answered. Was the LastCommon Ancestor of Metazoans radial-ly or bilaterally symmetrical? It wasneither, because it was both; just as itsdescendants were and are.

 Acknowledgments

I am grateful to Eric H. Davidson, Balazs

Papp, Douglas H. Erwin, and BernardM. Degnan for their helpful comments.I thank Marton Miskei for valuablediscussions, George Seel for checkingthe English, and   eye of science   forproviding the photo. I apologize to allthose whose work has not been cited

owing to the restriction in the number of references.

The author has declared no conflict of interest.

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Figure 1.   Radial and bilateral symmetry expressed in diverse levels of the body plan. (Water

bear,  Paramacrobiotus craterlaki ). Photo courtesy of “eye of science”.     eye of science.

G. Hollo

2   Bioessays 36: 0000–0000,   2014 WILEY Periodicals, Inc.

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