The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes
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RESEARCH
Open Access
The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes Marie-Therese Nödl1,4* , Alexandra Kerbl2, Manfred G. Walzl3, Gerd B. Müller1 and Heinz Gert de Couet4
Abstract Background: Cephalopods are a highly derived class of molluscs that adapted their body plan to a more active and predatory lifestyle. One intriguing adaptation is the modification of the ventral foot to form a bilaterally symmetric arm crown, which constitutes a true morphological novelty in evolution. In addition, this structure shows many diversifications within the class of cephalopods and therefore offers an interesting opportunity to study the molecular underpinnings of the emergence of phenotypic novelties and their diversification. Here we use the sepiolid Euprymna scolopes as a model to study the formation and differentiation of the decabrachian arm crown, which consists of four pairs of sessile arms and one pair of retractile tentacles. We provide a detailed description of arm crown formation in order to understand the basic morphology and the developmental dynamics of this structure. Results: We show that the morphological formation of the cephalopod appendages occurs during distinct phases, including outgrowth, elongation, and tissue differentiation. Early outgrowth is characterized by uniform cell proliferation, while the elongation of the appendages initiates tissue differentiation. The latter progresses in a gradient from proximal to distal, whereas cell proliferation becomes restricted to the distal-most end of the arm. Differences in the formation of arms and tentacles exist, with the tentacles showing an expedite growth rate and higher complexity at younger stages. Conclusion: The early outgrowth and differentiation of the E. scolopes arm crown shows similarities to the related, yet derived cephalopod Octopus vulgaris. Parallels in the growth and differentiation of appendages seem to exist throughout the animal kingdom, raising the question of whether these similarities reflect a recruitment of similar molecular patterning pathways. Keywords: Cephalopod, Euprymna scolopes, Bobtail squid, Lophotrochozoa, Arm crown, Appendage, Evolution, Development, Tentacle
Background Cephalopods represent a highly derived and very successful class within the phylum Mollusca, showing adaptations to all marine ecosystems from the deep sea to marine estuaries. They are thought to have evolved from a limpet-like monoplacophoran ancestor during the late Cambrian about 500 million years ago [1]. The eventual transition from a shell-bearing, bottom dwelling * Correspondence: [email protected] 1 Department of Theoretical Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria 4 Department of Biology, University of Hawaii at Manoa, 2538 McCarthy Mall, Edmondson Hall 413, Honolulu, HI 96822, USA Full list of author information is available at the end of the article
organism to a free-swimming, active predator was accompanied by the appearance of a serie
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