Regeneration mechanisms in Syllidae (Annelida)

Abstract

Syllidae is one of the most species-rich groups within Annelida, with a wide variety of reproductive modes and different regenerative processes. Syllids have striking ability to regenerate their body anteriorly and posteriorly, which in many species is redeployed during sexual (schizogamy) and asexual (fission) reproduction. This review summarizes the available data on regeneration in syllids, covering descriptions of regenerative mechanisms in different species as well as regeneration in relation to reproductive modes. Our survey shows that posterior regeneration is widely distributed in syllids, whereas anterior regeneration is limited in most of the species, excepting those reproducing by fission. The latter reproductive mode is well known for a few species belonging to Autolytinae, Eusyllinae, and Syllinae. Patterns of fission areas have been studied in these animals. Deviations of the regular regeneration pattern or aberrant forms such as bifurcated animals or individuals with multiple heads have been reported for several species. Some of these aberrations show a deviation of the bilateral symmetry and antero-posterior axis, which, interestingly, can also be observed in the regular branching body pattern of some species of syllids.

Keywords: annelid; epimorphosis; fission; morphallaxis; schizogamy.

Figure 1

Schematic drawing of the syllid body plan. Illustration of the main features in the morphology of a syllid: prostomium, segments, pygidium and digestive tube components, pharynx, pharyngeal tooth, proventricle, and intestine

Figure 2

Schematic representation of schizogamy in syllids. (A) Adult individual of a schizogamous species. Schizogamy can occur by scissiparity or gemmiparity. (B) Scissiparous individual during stolonization, based on Syllis spp. (Franke, 1999). (C) Gemmiparous individual during sequential gemmiparity based on Myrianida pachycera (Okada, 1933b). When the stolons are completely developed, they are detached for spawning. The stock animal regenerates the posterior body after the detachment of stolons. (D) Individual during posterior regeneration. (E) Male and female stolons perform spawning for exchange of gametes; scheme based on stolons of Syllis spp. (F) After spawning, stolons die. (G) Larval development in non‐brooding species; larvae disperse in ocean. (H) Alternatively, autolytine female stolons live during external brooding and development of the embryos; mature female carries an egg sack until the release of juveniles; ventral brooding; based on Myrianida pachycera (Okada, 1933b). (I) Growth of juveniles until mature stage to start a new stolonization process. pr, prostomium; py, pygidium; st, stolon

Figure 3

Distribution of some regenerative abilities and fragmentation in Syllidae. Regeneration data are based on reports of regenerating species and experimental studies (see Table 2). Presence and absence of regeneration was considered following, in general, categories by Zattara and Bely (2016), with some modifications: (1) axial regeneration absent (not even small portions of terminal tissue regenerate), (2) type I axial regeneration (caps can be regenerated after partial removal of these), (3) type II axial regeneration (caps, one or more segments and part of digestive tube can be regenerated), and (4) type III axial regeneration (like type II, but all digestive tube can be regenerated). Limited regeneration comprises inability to restore complete organs and extent comparable with the lost body before bisection, which includes type I and II axial categories. Type III was considered as presence of complete anterior or posterior regeneration. As suggested by Aguado, Glasby et al. (2015) and Aguado, Helm et al., (2015), Syllis and Typosyllis names remain as they were originally described. See Table 1 for data covering the information in this figure. AD, additional information; AR, anterior regeneration; PO, pharyngeal organ regeneration; PR, posterior regeneration. Phylogeny and distribution of reproductive modes following the most recent hypotheses (Aguado et al., 2012; Aguado, Glasby et al., 2015; Aguado, Helm et al., 2015)

Figure 4

Light microscope pictures of two regenerating species of syllids, Typosyllis antoni (A and C) (pictures by Michael Weidhase reproduced by permission) (Aguado, Glasby et al., 2015; Aguado, Helm et al., 2015), and Syllis sp. (B and D). (A) Anterior regeneration, 6 days after dissection (dad). (B) Early stages of posterior regeneration, pygidium and cirri present. (C) Posterior regeneration in 6 dad. (D) Growth stage of posterior regeneration. Dashed line represents the dissection region. All pictures are dorsal view. dtc, dorsal tentacular cirrus; ey, eye; ma, median antenna; mp, median papila; pc, pygidial cirrus; la, lateral antenna. Scale bar 250 μm

Figure 5

Different types of schizogamy: (A) scissiparity and (B)–(F) gemmiparity. (A) Scissiparous species Proceraea cornuta modified after Okada (1933a); a single stolon is produced per stolonization event. (B) Sequential gemmiparity in Myrianida sp., modified after Okada (1933b). (C). Successive budding in Trypanobia asterobia, modified after Okada (1933b). (D) Collateral budding in Trypanosyllis crosslandi Potts, 1911, modified after Potts (1911). (E) Collateral budding in Trypanedenta gemmipara (Johnson, 1901), modified after Johnson (1902). (F) Branching gemmiparity: branches and stolon in Syllis ramosa, modified after McIntosh (1885). All modified figures are in the public domain

Figure 6

Regeneration of Procerastea halleziana. (A) Adult specimen starting stolonization. (B) Specimen regenerating from three original segments of midbody. (C) Specimen regenerating from four original segments of midbody after defective fragmentation. (D) Aberrant specimen regenerating after fragmentation, there is a regenerate between two fragments; arrows point at putative SAZs. Modified from Allen (1923). All modified figures are in the public domain

Figure 7

Fragmentation series in species of three subfamilies of Syllidae. (A) Autolytinae, Procerastea halleziana, after Allen (1923, 1927a, 1927b). (B) Eusyllinae, Synmerosyllis lamelligera (Allen, 1927b). (C) Syllinae, Trypanosyllis zebra, after Okada (1929). (D) Autolytinae, Procerea picta, collected from Ferrol, Galicia, Spain; the method of intercalated addition of distilled water and seawater was performed with this specimen, following Allen (1923). Regions of constrictions are marked indicating their number of segments. The series obtained with the constriction regions is comparable to the fragmentation series described for this species, following the color pattern (Allen, 1927a; Okada, 1929). Formula characters: H, head; n, variable number of fragments; x, variable number of segments; P, pygidium. Scale bar 500 μm

Figure 8

Schematic drawings of anterior and posterior resegmentation in syllids. (A) Blastema formation; generalized scheme for Syllidae. (B) Anterior and posterior pattern of resegmentation based on eusyllines and syllines (Aguado, Helm et al., 2015; Boilly, 1961, 1967c; Weidhase, Beckers et al., 2016; Weidhase et al., 2017). (C) Anterior and posterior patterns of resegmentation based on the autolytine Procerastea halleziana (Allen, 1923). Establishment of posterior SAZ (B), (C). Anterior regeneration: a SAZ is not detectable (B) or takes place in the region immediately attached to the stock segment (C). SAZ, segment addition zone

Figure 9

Aberrant forms in some species of Syllidae. (A) Myrianida edwarsi: arrow point at tail regenerated in anterior end after transversal dissection; modified after Okada (1929). (B) Proceraea picta: double head regenerated after transversal dissection between 12th and 13th segment, modified after Okada (1929). (C) Syllis variegata: specimen with bifurcated anterior end; modified after Andrews (1892). (D) Procerastea halleziana: filled arrow point at additional parapodium laterally projected in the right side of 16th segment, empty arrow point at lateral regeneration in 19th segment, dorsal view, and (E) ventral view of the regenerate; modified after Allen (1923). (F) Myrianida ornata specimen with bifurcated posterior ends: arrow point at abnormal tail without cirri; modified after Andrews (1892). All modified figures are in the public domain