The simplicity of males: Dwarf males of four species of Osedax (Siboglinidae; Annelida) investigated by confocal laser scanning microscopy

Abstract

Dwarf males of the bone-eating worms Osedax (Siboglinidae, Annelida) have been proposed to develop from larvae that settle on females rather than on bone. The apparent arrest in somatic development and resemblance of the males to trochophore larvae has been posited as an example of paedomorphosis. Here, we present the first investigation of the entire muscle and nervous system in dwarf males of Osedax frankpressi, O. roseus, O. rubiplumus, and O. "spiral" analyzed by multistaining and confocal laser scanning microscopy. Sperm shape and spermiogenesis, the sperm duct and internal and external ciliary patterns were likewise visualized. The males of all four species possess morphological traits typical of newly settled siboglinid larvae: a prostomium, a peristomium with a prototroch, one elongate segment and a second shorter segment. Each segment has a ring of eight long-handled hooked chaetae. The longitudinal muscles are distributed as evenly spaced strands forming a grid with the thin outer circular muscles. Oblique protractor and retractor muscles are associated with each of the chaetal sacs. The nervous system comprises a cerebral ganglion, a prototroch nerve ring, paired dorsolateral longitudinal nerves, five ventral longitudinal nerves with paired, posterior ganglia and a terminal commissure, as well as a net of fine peripheral transverse plexuses surrounding the first segment. Internal ciliation occurs as paired ventrolateral bands along the first segment. The bands appear to lead the free mature sperm to a ciliated duct and seminal vesicle lying just behind the prototroch region. A duct then runs from the seminal vesicle into the dorsal part of the prostomium. The similarity of Osedax males to the larvae of Osedax and other siboglinid annelids as well as similarities shown here to the neuromuscular organization seen in other annelid larvae supports the hypothesis of paedomorphosis in males of Osedax.

An inordinate fondness for Osedax (Siboglinidae: Annelida): Fourteen new species of bone worms from California

“…are similar (Fig. 13) to the dwarfs found in other Osedax species (Worsaae & Rouse 2010), the anatomy of the females is unique among Osedax species and they show what appear to be striking adaptations to exploit bone fragments that have become buried in the sediment. Further study on the roots of Osedax jabba n. sp.…”

A Dwarf Male Reversal in Bone-Eating Worms

“…Collection details are in the Supplemental Information, as are light microscopy, histology, and confocal laser scanning microscopy protocols, which were published previously [13,14]. Specimens are lodged at the Benthic Invertebrate Collection at SIO.…”

“…Although resembling females, the males exhibit clear differences stemming from their ancestry as dwarfs. The dwarf males of other Osedax species reside in a female's tube and have free sperm in an anterior seminal vesicle [14,32]. In contrast, other siboglinids package their sperm [33,34].…”

External morphology of the cycliophoran dwarf male: a comparative study of Symbion pandora and S. americanus

“…The location of the penis inside a pouch is to our knowledge a new feature among metazoan dwarf males. In some cases, the penial structure is found inside the body (e.g., in polychaetes or monogonont rotifers; see Windoffer and Westheide 1988;Clément and Wurdak 1991) or may be entirely absent (e.g., in echiurans or the siboglinid Osedax; Schuchert and Rieger 1990; Rouse et al 2004;Worsaae and Rouse 2010). Therefore, more data are necessary to clarify the male-female interaction and the true function of the penial structure and the penial pouch.…”