The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes

Abstract

BackgroundCephalopods 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.ResultsWe 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.ConclusionThe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-016-0175-8) contains supplementary material, which is available to authorized users.

Pattern of sucker development in cuttlefishes

“…A few studies have been performed on the sucker development in squids and cuttle shes. In E. scolopes (Sepiolida), for example, it is reported that small undifferentiated suckers are observed on the oral side of the arm tip, indicating that new suckers are formed at the distal arm tip [20]. Together with our data, it is suggested that the patterns of sucker development are shared with Sepiida.…”

“…Since it was predicted that suckers were developed from undifferentiated buds to functional suckers with clear structures, observations on the external morphology and internal histological structures of cuttle sh arms during embryonic and postembryonic development were carried out to elucidate the pattern of sucker formation. Generally, in Coleoidea (octopuses, squids and cuttle shes), small suckers are located at the distal tips of arms, indicating that the new suckers are formed at the distal tips, as suggested in a few species [20,21]. In this study, therefore, the distal arm tips were focused on.…”

“…However, there are few studies focusing on the developmental process of sucker formation throughout these animals' lifetime. In the embryonic development of Euprymna scolopes (Sepiolida), small undifferentiated suckers were observed on the oral side of the arm tip, although the process of sucker development was not described in detail [20]. In some squid species belonging to Myopsida and Oegopsida, the processes of embryonic development were described (Illex illecebrosus: [22]; Sepioteuthis lessoniana: [23]; Dosidicus gigas: [24]; Todarodes paci cus: [25]), but the descriptions did not focus on sucker formation.…”

“…In this study, the body axes of embryos and arms were de ned according to the previous study (Fig. 1G, H) [20]. For postembryonic development, mantle length (ML) was utilized as a criterion of growth because the growth speed could be variable among individuals, so the time period elapsed during development is not suitable as a growth index [30,31].…”

Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

“…Morphological novelties in cephalopods include camera‐type eyes that evolved convergently with those found in vertebrates and flexible arms and tentacles that are thought to be derived from the molluscan foot . Together with the partial or complete loss of the molluscan shell, the arm crown has been proposed as a major morphological innovation for their diversification as it likely enabled these animals to become agile predators . Moreover, cephalopods have the largest nervous systems among invertebrates, rivaling vertebrates in terms of size and complexity .…”