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Juvenile Ontogeny and Metamorphosis in the Most Primitive Living Sessile Barnacle, Neoverruca, from Abyssal Hydrothermal Springs

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Juvenile Ontogeny and Metamorphosis in the Most Primitive Living Sessile Barnacle, Neoverruca, from Abyssal Hydrothermal Springs BULLETIN OF MARINE SCIENCE, 45(2): 467-477. 1989 JUVENILE ONTOGENY AND METAMORPHOSIS IN THE MOST PRIMITIVE LIVING SESSILE BARNACLE, NEOVERRUCA, FROM ABYSSAL HYDROTHERMAL SPRINGS William A. Newman ABSTRACT Neoverruca brachylepadoformis Newman recently described from abyssal hydrothermal springs at 3600 m in the Mariana Trough, has the basic organization of the most primitive sessile barnacles, the extinct Brachylepadomorpha (Jurassic-Miocene). However, a subtle asymmetry diagnostic of the Verrucomorpha (Cretaceous-Recent) is superimposed on this plan, and it is evident that Neoverruca also represents a very primitive verrucomorphan. A median latus, unpredicted in such a form, occurs on one side as part of the operculum, and the outermost whorl of basal imbricating plates is the oldest, rather than the youngest as in the primitive balanomorphans, Catophragmus s.1.and Chionelasmus and as inferred in Bra- chylepas. Neoverruca is further distinguished from higher sessile barnacles in passing through a number of well developed pedunculate stages before undergoing an abrupt metamorphosis into the sessile mode. Theses unpredicted ontogenetic events in the life history of an early sessile barnacle indicate that the transitory pedunculate stage of higher sessile barnacles, first noted in Semibalanus balanoides by Darwin, reflects the compression ofpedunculatejuvenile stages into a single stage, rather than simply a vestigial reminiscence of their pedunculate ancestry. From these observations it is evident that the transition from a pedunculate to a sessile way of life was evolutionarily more complicated than previously understood, and this has a significant bearing on our understanding of the paleoecology as well as the evolution of sessile barnacles. Abyssal hydrothermal vents have yielded two remarkable endemic barnacles, Neolepas zevinae Newman (1979) from approximately 2600 m, at 13° and 21°N on the East Pacific Rise, and Neoverruca brachylepadoformis in Newman and Hessler, 1989 from approximately 3600 m in the Mariana Trough in the western Pacific. The closest ancestors of Neolepas and Neoverruca, first appearing in the fossil record in the Mesozoic, have long been extinct and therefore Neolepas and Neoverruca are considered relics of Mesozoic age (Newman 1979; 1985; Newman and Hessler, 1989). McLean (1981, 1985) independently reached the same con- clusion concerning some hydrothermal vent gastropod mollusks. The capitular organization of Neolepas represents an early stage in the evolution of scalpellomorphan pedunculate barnacles; a stage intermediate between that of the simpler but extinct eolepadines and the more complexly armored pollicipe- dines (Buckeridge, 1979). The latter subfamily, represented today by Scillaelepas, Pollicipes and Capitulum, includes the inferred Mesozoic ancestor of all sessile barnacles (Brachylepadomorpha, Verrucomorpha and Balanomorpha; Newman, 1987, fig. 10E). Neoverruca is, in many ways, much more remarkable than Neolepas. It repre- sents the most primitive living sessile barnacle, and if there were no verruco- morphans, it would be classified as a slightly aberrant brachylepadomorphan. Indeed, as the sole surviving member of that radiation, it is a "living fossil." On the other hand, in light of the verrucomorphans, it constitutes the "missing link" between them and the extinct Brachylepadomorpha. Furthermore, some wholly unanticipated facets of the juvenile ontogeny, to be described below, further distinguish Neoverruca from other living sessile barnacles. These facets not only 467 468 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 require a reevaluation of our current understanding of metamorphosis in sessile barnacles, but our views concerning the evolution of sessility itself. JUVENILE ONTOGENY AND METAMORPHOSIS Neoverruca apparently passes through six or more pedunculate juvenile stages, but only a few were found associated with adults during the present study; several earlier and intermediate pedunculate stages are obviously missing from the se- quence presented here (Fig. I; see caption for symbols used to identify plates in the text). The pedunculate mode involves substantial growth as well as morpho- logical development and, therefore, must persist for a number of days before the abrupt metamorphosis into the sessile mode occurs. The earliest pedunculate stages observed are bilaterally symmetrical and similar in appearance to those of pollicipedine scalpellomorphans, including well devel- oped cirri by which they are apparently capable of feeding. Unfortunately, the youngest pedunculate juvenile stage known is not the first, but since it is bilaterally symmetrical (Fig. lA-B), younger ones must have been also. It has the usual five chitinous, primordial valves (S-T -C). However, as will be described, the median latus (L) is not the next plate to appear; rather, it appears heterochronously after several other calcareous plates, and then only on one side (Fig. 1D, F, H etc.). Thus there is no true Neolepas-stage (R-S-L-T-C, but see below) in Neoverruca, as there is in the pollicipedines and as was inferred in the early ontogeny of a brachylepadomorphan (Newman, 1987, fig. 9A). Further "irregularities" in the ordering of plates are observed in the early on- togeny of Neoverruca, but before proceeding it should be noted that all plates are designated "capitular," none "peduncular," for the reasons to be enumerated shortly. An explanation is necessary because the capitular plates of scalpellomor- phans, beyond the original five (S-T -C), are inferred to have been acquired phy- logenetically by transfer from the peduncle (Newman, 1982; 1987:35), and that such transfers occur ontogenetically was demonstrated by the development of subrostra in a species of Scillaelepas (Newman, 1980; fig. 11E, 0). These obser- vations could be relevant to the pedunculate stages of Neoverruca, but as it turns out they are not. The criteria applied in designating all plates of Neoverruca "capitular" stem simply from taking the ontogeny of the animal at face value (Fig. 1): 1)the division between the peduncle and capitulum in the pedunculate stages is well defined and the plates are wholly capitular in position, 2) the peduncle of all pedunculate stages remains naked, 3) the appearance ofL after 11indicates that the latter was capitular before the heterochrony developed, and 4) the appearance ofthe subsequent three whorls within the basic ring (Fig. 2), and then after the metamorphosis into the sessile mode, indicates that they are presently capitular, as they probably were before the positional anomaly was acquired. The naked peduncle is generally moderately short (Fig. lA-B and C-D), but when a cyprid larva settles in a deep crevice, the peduncle of the ensuing juvenile can be relatively long (Fig. IE-F). The capitular plates are deployed in two whorls (Fig. lA-B); the first, R-S-T-C, is normal, but the second is incomplete; sr-RL- "L," but no CL-sc. The first pair of latera to appear would appear to represent L. However, as shown below, it actually represents 11.The appearance of 11before L is heterochronous compared to pollicipedine, balanomorphan and presumably brachylepadomorphan ontogenies. In the next stage of two, CL appears on one side before it appears on the other (Fig. 10 vs. C and F vs. E), and this is the first sign of the developing asymmetry. L, A-J Figure 1. Ontogeny and metamorphosis in Neoverruca brachylepadoformis Newman: A-F, three pedunculate and G-L, four sessile ontogenetic stages. For ease of comparison both sides of an individual are illustrated as right sides. All individuals are from between crowded adults and therefore will bend over, or are bent over to the side that becomes the FS-Fr side. Notable features: I) the first stage illustrated is bilaterally symmetrical, 2) the second stage is becoming bilaterally asymmetrical in the number and arrangement of plates, 3) L appears after 1', 4) S and T become functionally FS-Fr, and MS-MT upon the acquisition of sessility, 5) transition from pedunculate to sessile (E-F to G-H) is highly metamorphic and, following acquisition of sessility, 6) RL and CL of the movable side join (albeit temporarily) before Rand C, 7) the subsequent three whorls of imbricating plates appear inside rather than outside the primary basal whorl, making the latter the outermost whorl, and 8) plates of the outcrmost whorl, especially I', sr and sc, become deciduous. From the cyprid to the first sessile stage apparently takes several days. (C, carina; c, imbricating plate carinad of L tier; CL, carinolatus; c1, imbricating plate in CL tier; FS, fixed scutum; Fr, fixed tergum; L, median latus; I, imbricating plate in L tier; MS, movable scutum; MT, movable tergum; R, rostrum; r, imbricating plate rostrad of L tier; RL, rostrolatus; rl, imbricating plate in RL tier; S, scutum; sc, subcarina; sr, subrostrum; T, tergum. Scale bars = I mm.) 470 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 The precocious side, marked by the appearance of CL (Fig. 1D, F etc.), is further distinguished by the appearance of L between the median basal angles of Sand T. Therefore, the precocious side is destined to be the relatively "normal," mov- able side; namely, that supporting MS-L-MT. While L is a relatively important plate in juveniles, its development becomes retarded in older individuals, and it is vestigial or even lost in old individuals (Newman and Hessler, 1989). The loss of normality on the movable side involves the meeting of the lateral margins of Rand C, but the meeting is preceded by the transient meeting of RL and CL (Fig. IH, J). On the opposite side L fails to appear; the basal margins of Sand T are relatively wide and remain between Rand C where they eventually become immovably "fixed" (FS-FT). These deletions and readjustments are con- cerned more with the developing, fundamental, verrucomorphan apomorphies than with the impending metamorphosis from the pedunculate to the sessile mode per se. The complete second or basal whorl consists of 8 plates (sr-RL-P-CL-sc; Fig. 2), and with its completion the last pedunculate stage is ready to undergo an abrupt metamorphosis into the first sessile stage (Fig.
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