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The Evolutionary Origin of Digit Patterning Touro Scholar NYMC Faculty Publications Faculty 11-1-2017 The Evolutionary Origin of Digit Patterning T Stewart Ramray Bhat Stuart Newman New York Medical College Follow this and additional works at: https://touroscholar.touro.edu/nymc_fac_pubs Part of the Developmental Biology Commons, and the Medicine and Health Sciences Commons Recommended Citation Stewart, T., Bhat, R., & Newman, S. (2017). The Evolutionary Origin of Digit Patterning. EvoDevo, 8, 21. https://doi.org/10.1186/s13227-017-0084-8 This Article is brought to you for free and open access by the Faculty at Touro Scholar. It has been accepted for inclusion in NYMC Faculty Publications by an authorized administrator of Touro Scholar. For more information, please contact [email protected]. Stewart et al. EvoDevo (2017) 8:21 DOI 10.1186/s13227-017-0084-8 EvoDevo REVIEW Open Access The evolutionary origin of digit patterning Thomas A. Stewart1,2,5*, Ramray Bhat3 and Stuart A. Newman4 Abstract The evolution of tetrapod limbs from paired fns has long been of interest to both evolutionary and developmental biologists. Several recent investigative tracks have converged to restructure hypotheses in this area. First, there is now general agreement that the limb skeleton is patterned by one or more Turing-type reaction–difusion, or reaction–dif- fusion–adhesion, mechanism that involves the dynamical breaking of spatial symmetry. Second, experimental studies in fnned vertebrates, such as catshark and zebrafsh, have disclosed unexpected correspondence between the devel- opment of digits and the development of both the endoskeleton and the dermal skeleton of fns. Finally, detailed mathematical models in conjunction with analyses of the evolution of putative Turing system components have permitted formulation of scenarios for the stepwise evolutionary origin of patterning networks in the tetrapod limb. The confuence of experimental and biological physics approaches in conjunction with deepening understanding of the developmental genetics of paired fns and limbs has moved the feld closer to understanding the fn-to-limb transition. We indicate challenges posed by still unresolved issues of novelty, homology, and the relation between cell diferentiation and pattern formation. Keywords: Development, Fin, Genetics, Novelty, Turing, Self-organization Background Digits develop in a domain of the limb bud marked by Te appearance of tetrapods in the Late Devonian [1–3] late-phase expression of Hoxa13 and Hoxd13 [7, 8] and marked a major transition in life’s history, foreshadowing a the absence of Hoxa11, which is expressed more proxi- restructuring of the earth’s ecosystems. Tetrapods are now mally [9]. Previously, late-phase Hox expression was abundant in terrestrial, aerial, and aquatic environments, taken as a hallmark of the autopod, and digit origin was and they include both the largest and smallest living adult therefore attributed to the evolution of a new gene regu- vertebrates [4, 5]. Likely key to this radiation was the origi- latory state in the distal limb-bud mesenchyme [10, 11]. nation and diversifcation of limbs. Te limbs of tetrapods However, reevaluation of actinopterygian [12–14], chon- evolved from paired fns, and they can be diagnosed by the drichthyan [15], and sarcopterygian [16] paired fn devel- absence of dermal skeleton (lepidotrichia) and the presence opment revealed patterns of Hox gene expression similar of digits, which are parallel, non-branching and segmented to the late phase of limbs. Tese patterns are driven in endoskeletal elements at the distal end of vertebrate paired fns and limbs by conserved gene regulatory elements pectoral and pelvic appendages (Fig. 1) [6]. Over the past [17, 18]. Most recently, cell lineage tracing and the appli- few years, hypotheses of how limbs evolved from fns cation of CRISPR/Cas9 editing in zebrafsh (Danio rerio) have been restructured dramatically. Tis progress refects showed that Hox13-expressing cells of the distal mesen- greater understanding of both the evolution of gene regula- chyme in paired fns form the dermal fn skeleton [19]. tion and the role of Turing-type self-organizing systems in Tus, digit origin appears to have involved eliciting new the patterning of condensing limb-bud mesenchyme. or latent chondrogenic potential of the Hox13-express- ing cells, transforming the fate and patterning of this *Correspondence: [email protected] compartment of distal fn mesenchyme from fn rays to 1 Department of Ecology and Evolutionary Biology, Yale University, 300 digits. Loss of the embryonic fn fold in paired append- Hefernan Dr, West Haven, CT 06515, USA Full list of author information is available at the end of the article ages might have contributed to this transformation; if © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Stewart et al. EvoDevo (2017) 8:21 Page 2 of 7 abc acropod lepidotrichia autopod mesopod zeugopod digits stylopod radius ulna humerus Tiktaalik rosae † Acanthostega gunnari † Homo sapiens Fig. 1 Fin-to-limb transition involved a suite of anatomical changes including loss of dermal fn rays and the acquisition of digits. a Pectoral fn skeleton of Tiktaalik roseae, an elpistostegid fsh. The fn contains both dermal skeleton (lepidotrichia) and endochondral skeleton. Illustration modifed from Shubin et al. [64]. b Forelimb skeleton of Acanthostega gunnari, a stem tetrapod. The limb exhibits a polydactylous pattern, which is characteristic of the earliest limbs. Illustration modifed from Coates et al. [65] follows that labeling scheme, although other labeling schemes have been proposed for autopodial elements (e.g., [66]). c Forelimb skeleton of human (Homo sapiens). This limb shows a pentadactyl pattern and also mesopodial (wrist) elements; these features characterize the crown-group tetrapod condition. Illustration modifed from Owen [67]. For each illustration, anterior is oriented to the left. Extinct taxa are noted with a dagger (†) mesenchymal cells could no longer migrate into the fn phenomena such as the pigment stripes on a zebra’s skin fold, then they would have remained in a terminal posi- and the seed spirals of the sunfower’s face. Te class of tion within the fn bud and in a developmental context mechanisms he advanced was based on simple chemis- that promotes diferentiation into endoskeleton [12]. try and physics, reaction and difusion, but led to spatial Te limb skeleton develops by the condensation distributions of reagents and products that, counterintui- of mesenchyme in the limb bud [20]. Te stylopod tively, exhibited reproducible spatial non-uniformities. A (humerus/femur) forms frst, followed by the zeugopod straightforward way this can occur is if a chemical that (ulna and radius/tibia and fbula), and fnally the auto- activates its own production difuses from its site of pro- pod (the wrist/ankle and digits). Beginning in the 1970s, duction more slowly than a second chemical, which is models for limb development were proposed that pre- also produced in response to the frst. If the second mol- dicted that the patterning of the limb skeleton had a ecule inhibits the initial auto-activating reaction, it will causal basis in reaction–difusion phenomena [21, 22] act as a “lateral inhibitor,” causing centers of production famously expounded by the mathematician A.M. Turing to form in a spatially separated fashion. Rates of reaction in a 1952 paper, “Te Chemical Basis of Morphogenesis” and difusion defne the magnitude of this spacing, which [23]. In this paper, we review how Turing-type models (under an appropriate range of conditions) will be regu- are being used to explain the fn-to-limb transition. We lar: a “chemical wavelength.” also indicate future research strategies aforded by these Te recognition that the change of cell state (e.g., models and explore the conceptual implications of inte- determination and diferentiation), along with secre- grating approaches from biological physics and develop- tion of proteins and other molecules, provides a biologi- mental genetics to the questions of limb origination and cal analogue of a chemical reaction, while any transport evolution. of molecules across a tissue can be treated formally like difusion, helped connect experimental developmental Turing‑type mechanisms of pattern formation genetics to abstract mathematics. Moreover, as Mein- Toward the end of his life, the computer science pioneer hardt noted [24], activator–inhibitor networks described A.M. Turing published a paper [23] that addressed an above are not the only mode by which reaction–difusion unconventional side-interest of his—biological patterns, systems can break spatial uniformity and create patterns. Stewart et al. EvoDevo (2017) 8:21 Page 3 of 7 Substrate–depletion networks employ the local break- pectoral fns of the catshark (Scyliorhinus canicula) down of a precursor of the autocatalytic activator as the showed it to be integral to the formation of an array of causal basis of the spacing of primordia. Other network cartilage
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