Pattern of sucker development in cuttlefishes

Abstract

Background: Morphological novelties have been acquired through evolutionary processes and related to the adaptation of new life-history strategies with new functions of the bodyparts. Cephalopod molluscs such as octopuses, squids and cuttlefishes possess unique morphological characteristics. Among those novel morphologies, in particular, suckers arranged along the oral side of each arm possess multiple functions, such as capturing prey and locomotion, so that the sucker morphology is diversified among species, depending on their ecological niche. However, the detailed developmental process of sucker formation has remained unclear, although it is known that new suckers are formed or added during both embryonic and postembryonic development. In the present study, therefore, focusing on two cuttlefish species, Sepia esculenta and S. lycidas, in which the sucker morphology is relatively simple, morphological and histological observations were carried out during embryonic and postembryonic development to elucidate the developmental process of sucker formation and to compare them among other cephalopod species. Results: The observations in both species clearly showed that the newly formed suckers were added on the oral side of the most distal tip of each arm during embryonic and postembryonic development. On the oral side of the arm tip, the epithelial tissue became swollen to form a ridge along the proximal-distal axis (sucker field ridge). Next to the sucker field ridge, there were small dome-shaped bulges that are presumed to be the sucker buds. Toward the proximal direction, the buds became functional suckers, in which the inner tissues differentiated to form the complex sucker structures. During postembryonic development, on both sides of the sucker field ridge, epithelial tissues extended to form a sheath, covering the ridge for protection of undifferentiated suckers. Conclusions: The developmental process of sucker formation, in which sucker buds are generated from a ridge structure (sucker field ridge) on the oral side at the distal-most arm tip, was shared in both cuttlefish species, although some minor heterochronic shifts of the developmental events were detected between the two species.

Evolutionary development of the cephalopod arm armature: a review

“…Chitins have so far been analysed only in gladiuses, beaks, and in the sucker surfaces of octopods. At least, in hematoxylin and eosin-stained sections of post-embryonal Sepia , both the sucker ring and the adjacent infundibulum exhibit the same colour (see Kimbara et al, 2020 , Fig. 5 L) suggesting a similar acidophil composition.…”

Sucker formation in a bigfin reef squid: Comparison between arms and tentacles

“…Fixation and fluorescent staining were performed for observations under a confocal laser‐scanning microscope (CLSM) according to previous studies (Kimbara et al, 2020; Oguchi et al, 2016). Briefly, embryos at each developmental stage (St. 22–29) and juveniles (ML = 15–30 mm) were fixed in PFA‐FSW fixative for more than 3 h after they were anesthetized with 3.5% MgCl 2 .…”

“…Furthermore, although sucker structures and the number of sucker rows are varied among species in Decapodiformes (Nixon & Dilly, 1977; Okutani, 2015), it has not been revealed how sucker morphologies have diversified from the ancestral state because there is little information on sucker development in ancestral squids/cuttlefishes. Detailed information on the sucker‐formation patterns on arms throughout embryonic and postembryonic development is restricted to cuttlefishes, that is, Sepiida (Kimbara et al, 2020), so that other squid lineages should also be investigated to elucidate the evolutionary patterns of suckers in Decapodiformes. Since Sepiida and Myopsida are distinct lineages in the Decapodiformes phylogeny (Lindgren & Anderson, 2018; Strugnell et al, 2017; Tanner et al, 2017; Uribe & Zardoya, 2017), comparison between Sepiida and Myopsida might reveal the shared sucker formation pattern among squids and cuttlefishes.…”

“…In this study, therefore, focusing on the squid species Sepioteuthis lessoniana Férussac, 1831 in Lesson (1830–1831) (Myopsida), morphological and histological observations of sucker‐formation processes were carried out in arms and tentacles during embryonic through postembryonic development to reveal the sucker‐formation processes producing the tentacle‐specific morphologies. Those processes were also compared with the previously described sucker development in cuttlefishes (Kimbara et al, 2020; Tarazona et al, 2019). Among squid arms, second arms are focused in this study because they are simplest arms, while other arms exhibit specialized morphologies like swimming membranes.…”

“…Among squid arms, second arms are focused in this study because they are simplest arms, while other arms exhibit specialized morphologies like swimming membranes. For this reason, some previous researchers especially focused on second arms for developmental descriptions (Kimbara et al, 2020; Nödl et al, 2016).…”