Development, organization, and remodeling of phoronid muscles from embryo to metamorphosis (Lophotrochozoa: Phoronida)

Abstract

BackgroundThe phoronid larva, which is called the actinotrocha, is one of the most remarkable planktotrophic larval types among marine invertebrates. Actinotrochs live in plankton for relatively long periods and undergo catastrophic metamorphosis, in which some parts of the larval body are consumed by the juvenile. The development and organization of the muscular system has never been described in detail for actinotrochs and for other stages in the phoronid life cycle.ResultsIn Phoronopsis harmeri, muscular elements of the preoral lobe and the collar originate in the mid-gastrula stage from mesodermal cells, which have immigrated from the anterior wall of the archenteron. Muscles of the trunk originate from posterior mesoderm together with the trunk coelom. The organization of the muscular system in phoronid larvae of different species is very complex and consists of 14 groups of muscles. The telotroch constrictor, which holds the telotroch in the larval body during metamorphosis, is described for the first time. This unusual muscle is formed by apical myofilaments of the epidermal cells. Most larval muscles are formed by cells with cross-striated organization of myofibrils. During metamorphosis, most elements of the larval muscular system degenerate, but some of them remain and are integrated into the juvenile musculature.ConclusionEarly steps of phoronid myogenesis reflect the peculiarities of the actinotroch larva: the muscle of the preoral lobe is the first muscle to appear, and it is important for food capture. The larval muscular system is organized in differently in different phoronid larvae, but always exhibits a complexity that probably results from the long pelagic life, planktotrophy, and catastrophic metamorphosis. Degeneration of the larval muscular system during phoronid metamorphosis occurs in two ways, i.e., by complete or by incomplete destruction of larval muscular elements. The organization and remodeling of the muscular system in phoronids exhibits the combination of protostome-like and deuterostome-like features. This combination, which has also been found in the organization of some other systems in phoronids, can be regarded as an important characteristic and one that probably reflects the basal position of phoronids within the Lophotrochozoa.

Phoronida

“…In this species, the larval tentacle muscles (both elevators and depressors) are broken down and new juvenile tentacle muscles are formed in a day (Santagata 2002 ). However, in Phoronopsis harmeri , only the tentacle depressors are broken down (Temereva and Tsitrin 2013 ), and this difference may be linked with the fact that the tentacle capillaries are already formed and expanded in the competent larva's comparatively larger tentacles. Other muscles carried over to the juvenile body in this species are found in the esophagus (Temereva and Tsitrin 2013 ).…”

“…The trunk sac continues to elongate, displacing the stomach and intestine dorsally. The trunk sac differentiates into what will be the trunk epithelium of the juvenile, replete with numerous circular and longitudinal muscles (Zimmer 1964 ;Santagata 2002 ;Temereva and Tsitrin 2013 ). Other general features of the competent actinotroch larva are the compact mass(es) of red blood cells that form in the collar region ( Fig.…”

“…10.3H ). During this process, the cells of the blood corpuscle mass dissociate and stream into the vessels of the juvenile circulatory system (Zimmer 1991 ;Santagata 2002 ;Temereva and Tsitrin 2013 ). Depending on how the juvenile tentacles develop (Santagata and Zimmer 2002 ), there are differences in (1) the formation of the lophophore blood vessels and (2) the larval tissues that undergo cell death.…”

“…Once released from the parental tube, Phoronis ovalis larvae swim in the plankton for about 4 days and then transition to a demersal phase, swimming near the bottom for about 3 days before undergoing metamorphosis (Silén 1954b ;Zimmer 1991 ). Feeding actinotroch larvae have a complex complement of striated musculature for lifting and closing the preoral hood; extending, fl icking, or lowering the tentacles; and adjusting the angle of the teletrochal band of cilia while swimming (Zimmer 1964 ;Santagata and Zimmer 2002 ;Santagata 2002Santagata , 2004bTemereva and Tsitrin 2013 ). Although many aspects of larval musculature are shared among several phoronid species, the morphology of particular larval muscles does differ, especially when considering the smaller and more compact actinotroch types ( P. pallida , P. ijimai , and P. hippocrepia ) as opposed to the larger and more elongate types ( Phoronopsis harmeri and Phoronis muelleri ; see Santagata and Zimmer 2002 ;Temereva and Tsitrin 2013 ).…”

“…Mesenchymal cells now line the subumbrellar portion of the hood and the ectodermal portion of the trunk. These cells differentiate into muscle cells that form the initial body wall muscle fi bers of the larva (Santagata 2004b ;Temereva and Tsitrin 2013 ). Where the blind-ended gut meets the posterior ectoderm, the anus and intestine form from an ectodermal invagination (Freeman and Martindale 2002 ).…”